See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/365999889

Impacts of Salinity Stress on Plants and Their Tolerance Strategies: A Review

Article in Middle East Journal of Applied Sciences · July 2022

DOI: 10.36632/mejas/2022.12.3.27

CITATIONS READS
5 1,924

5 authors, including:

El-Zanaty Abd El-Motaleb Aly Abou El-Nour Hala El-Bassiouny

National Research Centre, Egypt National Research Center, Egypt
71 PUBLICATIONS 688 CITATIONS 38 PUBLICATIONS 1,344 CITATIONS

SEE PROFILE SEE PROFILE

All content following this page was uploaded by El-Zanaty Abd El-Motaleb Aly Abou El-Nour on 04 December 2022.

The user has requested enhancement of the downloaded file.

 Middle East Journal of Applied Sciences
Volume: 12 | Issue: 03| July – Sept. | 2022
EISSN: 2706 -7947 ISSN: 2077- 4613
DOI: 10.36632/mejas/2022.12.3.27
Journal homepage: www.curresweb.com
Pages: 282-400

Impacts of Salinity Stress on Plants and Their Tolerance Strategies: A Review

Abou Seeda M.A.1, 2E.A.A. Abou El-Nour, 3Maha M.S. Abdallah, 3Hala M.S. El-
Bassiouny and 3Abd El-Monem A.A.
1
Plant Nutrition Dept., 2 Fertilization Technology Dept., and 3Botany Dept., National Research Centre,
33 El-Buhouth St. Dokki, Giza, P.O. 12622 Egypt.
Received: 20 July 2022 Accepted: 22 Sept. 2022 Published: 30 Sept. 2022

ABSTRACT
The environmental stress is a major area of scientific concern because it constraints plant as well as
crop productivity. This situation has been further worsened by anthropogenic activities. Salinity is a
major abiotic stress limiting growth and productivity of plants in many areas of the world due to
increasing use of poor quality of water for irrigation and soil salinization. Plant adaptation or tolerance
to salinity stress involves complex physiological traits, metabolic pathways, and molecular or gene
networks. A comprehensive understanding on how plants respond to salinity stress at different levels
and an integrated approach of combining molecular tools with physiological and biochemical
techniques are imperative for the development of salt-tolerant varieties of plants in salt-affected areas.
Salt stress causes decrease in plant growth and productivity by disrupting physiological processes,
especially photosynthesis. The accumulation of intracellular sodium ions at salt stress changes the ratio
of K: Na, which seems to affect the bio energetic processes of photosynthesis. Here, we review recent
discoveries on regulatory systems that link sensing and signaling of these environmental cues focusing
on the integrative function of transcription activators. Key components that control and modulate stress
adaptive pathways include transcription factors (TFs) ranging from bZIP, AP2/ERF, and MYB proteins
to general TFs. Recent studies indicate that molecular dynamics as specific homodimerizations and
eterodimerizations as well as modular flexibility and posttranslational modifications determine the
functional specificity of TFs in environmental adaptation. Function of central regulators as NAC,
WRKY, and zinc finger proteins may be modulated by mechanisms as small RNA (miRNA)-mediated
posttranscriptional silencing and reactive oxygen species signaling. In addition to the key function of
hub factors of stress tolerance within hierarchical regulatory networks, epigenetic processes as DNA
methylation and posttranslational modifications of histones highly influence the efficiency of stress-
induced gene expression. Comprehensive elucidation of dynamic coordination of drought and salt
responsive TFs in interacting pathways and their specific integration in the cellular network of stress
adaptation will provide new opportunities for the engineering of plant tolerance to these environmental
stressors.

Keywords: genomics, metabolomics, plant productivity, proteomics, salinity stress, salinity tolerance,
transcriptomics
1. Introduction
Stress is defined as any external abiotic (salinity, heat, water, etc.) or biotic (herbivore) constraint
that limits the rate of photosynthesis and reduces a plant’s ability to convert energy to biomass Grime,
(1977). A major challenge towards world agriculture involves production of 70% more food crop for
an additional 2.3 billion people by 2050 worldwide FAO, (2009). Salinity is a major stress limiting the
increase in the demand for food crops. More than 20% of cultivated land worldwide (∼ about 45
hectares) is affected by salt stress and the amount is increasing day by day. Plants because of adaptive
evolution can be classified roughly into two major types: the halophytes (that can withstand salinity)
and the glycophytes (that cannot withstand salinity and eventually die). Majority of major crop species
belong to this second category. Thus salinity is one of the most brutal environmental stresses that
Corresponding Author: Abou Seeda M.A, National Research Centre, 33 El-Buhouth St. Dokki, Giza, P.O.
12622 Egypt. E-mail: mabouseeda@gmail.com
282
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

hamper crop productivity worldwide Flowers, (2004); Munns and Tester, (2008). Salinity stress
involves changes in various physiological and metabolic processes, depending on severity and duration
of the stress, and ultimately inhibits crop production James et al., (2011); Rozema and Flowers, (2008).
Soil salinity is known to represses plant growth in the form of osmotic stress that is then followed by
ion toxicity James et al., (2011); Rahnama et al., (2010). During the initial phases of salinity stress,
water absorption capacity of root systems decreases and water loss from leaves is accelerated due to
osmotic stress of high salt, accumulation in soil and plants, and therefore salinity stress is also
considered as hyperosmotic stress Munns, (2005) Fig. (1) .

Fig. 1: Salinity stress induced osmotic stress tolerance mechanisms in plants. Increase in salt in soil
lowers the soil water potential of plant cells. This reduces water uptake by plants and consequently
causes cellular dehydration (1) (left). To combat this issue, plants accumulate osmolytes, such as
proline, sugars and polyamines in higher concentration. Osmolyte accumulation results in lowering of
cellular water potential and maintains a favorable gradient for water uptake from soil to roots.
Endophytic fungi alleviate osmotic stress by influencing the expression of specific genes, P5CS,
pyroline-5-carboxylate synthase (1a) (right), involved in the biosynthesis of the osmolyte proline,
activation of starch degrading enzyme, glucan-water dikinase (1b) (right) and forming tripartite
symbiosis with roots and rhizobia (1c) (right) to elevate the accumulation of sugars and by increasing
the biosynthesis of polyamines such as spermidine and spermine (1D) (right). See text for relevant
references and further details

Osmotic stress in the initial stage of salinity stress causes various physiological changes, such as
interruption of membranes, nutrient imbalance, impairs the ability to detoxify reactive oxygen species
(ROS), differences in the antioxidant enzymes and decreased photosynthetic activity, and decrease in
stomatal aperture Munns and Tester, (2008), Rahnama et al., (2010) Fig. (2). Salinity stress is also
considered as a hyperionic stress. One of the most detrimental effects of salinity stress is the
accumulation of Na+ and Cl− ions in tissues of plants exposed to soils with high NaCl concentrations.
Entry of both Na+ and Cl− into the cells causes severe ion imbalance and excess uptake might cause
significant physiological disorder(s). High Na+ concentration inhibits uptake of K+ ions which is an
essential element for growth and development that results into lower productivity and may even lead to
death James et al., (2011)

283
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 2: Schematic model showing the effects of salinity in potato. Salt stress causes visible
morphological changes such as leaf aging, premature, senescence and decline in root growth. It
interferes with the osmotic balance due to the accumulation of toxic ions. Toxic ions lead to cellular
interference and ROS generation that causes plasma membrane disruption, hindrance to respiration and
damage to enzyme structure. These ions cause deficiency of essential nutrients and their imbalance. Salt
stress also causes osmotic stress that leads to water imbalance and due to which closure of stomata and
reduction of water potential occurs. After Kumar et al., (2021)

In response to salinity stress, the production of ROS, such as singlet oxygen, superoxide,
hydroxyl radical, and hydrogen peroxide, is enhanced Apel and Hirt, (2004), Ahmad and Umar, (2011).
Salinity-induced ROS formation can lead to oxidative damages in various cellular components such as
proteins, lipids, and DNA, interrupting vital cellular functions of plants. Genetic variations in salt
tolerance exist, and the degree of salt tolerance varies with plant species and varieties within a species.
Amongmajor crops, barley (Hordeumvulgare) shows a greater degree of salt tolerance than rice (Oryza
sativa) and wheat (Triticum aestivum). The degree of variation is even more pronounced in the case of
dicotyledons ranging from Arabidopsis thaliana, which is very sensitive towards salinity, to halophytes
such as Mesembryanthemum crystallinum, Atriplex sp., Thellungiella salsuginea (previously known as
T. halophila) Munns and Tester, (2008), Pang et al., (2010), Abrah´am et al., (2011). In the last two
decades, sumptuous amount of research has been done in order to understand the mechanism of salt
tolerance in model plant Arabidopsis Zhang and Shi, (2013). Genetic variations and differential
responses to salinity stress in plants differing in stress tolerance enable plant biologists to identify
physiological mechanisms, sets of genes, and gene products that are involved in increasing stress
tolerance and to incorporate them in suitable species to yield salt tolerant varieties.

2. Causes of salinity
2.1. Natural cause
Most of the saline Sodic soils are developed due to natural geological, hydrological and
Pedological processes. Some of the parent materials of those soils include intermediate igneous rocks
such as phenolytes, basic igneous rocks such as basalt, undifferentiated volcanic rocks, sandstones,
alluvium and lagoonal deposits Wanjogu et al., (2001). Climatic factors and water management may
accelerate salinization. In arid and semi-arid lands, evapo-transpiration plays a very important role in
the pedogenesis of saline and sodic soils Fig. (3).

284
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 3: Soil salinity under climate change: Challenges for sustainable agriculture and food security

Another type of salinity occurs in coastal areas subjected to tides and the main cause is intrusion
of saline water into rivers Cyrus et al., (1997) or aquifers Howard and Mullings, (1996). Coastal rice
crops in Asia, for instance, are frequently affected by exposure to seawater brought in by cyclones
around the Indian Ocean Sultana et al., (2001). Cyclic salts are ocean salts carried inland by wind and
deposited by rainfall, and are mainly sodium chloride Fig. (4).

Fig. 4: Current processes leading to salinization. Sea-level rise and extreme events promote seawater
flooding and intrusion into coastal land that leads to deforestation. Deforestation can result in increased
rates of evaporation that brings salt to the surface layers of the soil and catalyse deforestation and soil
fertility reduction. Human practices can induce salinization through deforestation, effluent discharge
and water-table rise that may bring salts to the top layers of the soil. High temperatures lead to increased
evaporation and other extreme events can cause atmospheric deposition of salts. After Rocha et al.,
(2020)

Depending on prevailing winds and distance from the seacoast, the rainwater composition greatly
varies. The composition of seawater is expressed as g kg-1 or ppt (parts per thousands) and is almost
uniform around the globe. The electrical conductivity of seawater is 55 dS m-1 while that of rainwater
is about 0.01 dS m-1.

2.2. Anthropogenically induced salinity

Secondary salt affected soils are those that have been salinized by human caused factors, mainly
because of improper methods of irrigation. Poor quality water is often used for irrigation, so that
eventually salt builds up in the soil unless the management of the irrigation system is such that salts are
leached from the soil profile. Szaboles, (1992); Garg and Manchanda, (2008) estimated that 50% of all
irrigated schemes are salt affected. Too few attempts have been made recently to access the degree of

285
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

human-induced secondary salinization and, according to Flowers and Yeo, (1995); this makes it
difficult to evaluate the importance of salinity to future agricultural productivity. Nevertheless,
Ponnamperuma, (1984) has reported increasing salinization with increasing irrigation since 1950’s and
in the Shansa Province in China, more than one third of the total area of irrigated land is salinized Qiao,
(1995). Anthropic salinization occurs in arid and semi-arid areas due to waterlogging brought about by
improper irrigation Ponnamperuma, (1984). Secondary salt affected soils can also be caused by human
activities other than irrigation and include, but are not limited to the following:

2.2.1. Deforestation
It is recognized as a major cause of salinization and alkalization of soils because of the effects of
salt migration in both the upper and lower layers. Deforestation leads to the reduction in average rainfall
and increased surface temperature Hastenrath, (1991); Shukla, (1990). Top thin soil rapidly is eroded
in the absence of soil green cover. Without the trees there to act as a buffer between the soil and the
rain, erosion is practically inevitable. Soil erosion then leads to greater amounts of run-off and increased
sedimentation in the rivers and streams. The combination of these factors leads to flooding and
increased salinity of the soil Domries, (1991); Hastenrath, (1991). The Indian plains formed by the
rivers of north India increasingly getting salt affected as coastal areas of Ganges particularly lower
Ganges plains and Sundarban estuarine areas. In southeast India, for example, vast areas of farmer
forestland became increasingly saline and alkaline within a few years after the felling of the woods
Szaboles, (1994). In Australia, a country where one-third of the soils are Sodic and 5% saline
Fitzpatrick, (1994), there is serious risk of salinization if land with shallow unconfined aquifers
containing water with more than 0.25% total soluble salt is decreased of trees Bui et al., (1996).

2.2.2. Accumulation of air-borne or water-borne salts in soils

Szaboles, (1994) has reported that chemicals from industrial emissions may accumulate in the
soil, and if the concentration is high enough, can result in salt accumulation in the upper layer of soil.
Similarly, water with considerable salt concentration such as wastewater from municipalities and sludge
may contaminate the upper soil later causing salinization and/or alkalization Bond, (1998)

2.2.3. Contamination with chemicals

It often occurs in modern intensive agricultural systems, particularly in green houses and
intensive farming systems.

2.2.4. Overgrazing
This process occurs mainly in arid and semi-arid regions, where the natural soil cover is poor and
scarcely satisfies the fodder requirement of intensive animal husbandry Szaboles, (1994). The natural
vegetation becomes sparse and progressive salinization develops, and sometimes the process ends up
in desertification as the pasture diminishes due to overgrazing. Factors modifying the salinity: The
severity of secondary salinity arises when salt stored in the soil profile or groundwater is mobilized and
enters the root zone. It happens often when extra water reaches the system due to irrigation or other
human activities, viz. deforestation and land clearing. Extra water raises water tables or increases
pressures in areas confined or affected by primary salinity particularly in arid and semiarid regions.
Their condition varies in severity from slight salinity with little effect on plant growth to severe salinity
where semi-confined aquifers causing the upward movement of water to the soil surface. Saline water
from deep aquifers or salt deposits from deep soil horizons can move upwards with the rising water.
When the water table comes near or reaches the soil surface, appreciable upward movement of water
occurs due to evaporation from the soil surface and salts accumulate in the root zone Abrol, (1986).
Beyond the threshold level of the water table, the rate of evaporation and associated salinization increase
rapidly. The high temperature conditions often exaggerate these conditions. Different soil types have
different threshold levels, but these are commonly reached in irrigated situations. Secondary salinization
can also occur due to the use of inadequate quantities of irrigation water to leach salts that accumulate
in the root zone due to evaporation Umali, (1993). It was realized that the reaction of crops to saline
irrigation water was affected not only by the salinity level but also by soil characteristics, irrigation
practices such as the type of system and timing and the amount of irrigation applications. Moreover,
different crop varieties react differently. Whether to use irrigation water of marginal quality would also

286
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

depend on the level of yield reduction one is prepared to accept Rhoades and Loveday, (1990). For
conventional surface irrigation, and a leaching fraction of 0.1 (i.e. 10% more water than is needed to
satisfy the crop evaporative demand), water salinity should not exceed 1dS m-1 for sensitive crops. For
moderately sensitive, the threshold is 1.8 dS m-1; for moderately tolerant, 3.3 dS m-1; and for tolerant
crops, 5.8 dS m-1. In each of these categories, water of higher salinity would lead to yield decline. Higher
leaching fractions move the threshold value up, but by how much, depends on the circumstances
Rhoades and Loveday, (1990).

3. Factors modifying the salinity

The severity of secondary salinity arises when salt stored in the soil profile or groundwater is
mobilized and enters the root zone. It happens often when extra water reaches the system due to
irrigation or other human activities, viz. deforestation and land clearing. Extra water raises water tables
or increases pressures in areas confined or affected by primary salinity particularly in arid and semiarid
regions. Their condition varies in severity from slight salinity with little effect on plant growth to severe
salinity where semi-confined aquifers causing the upward movement of water to the soil surface. Saline
water from deep aquifers or salt deposits from deep soil horizons can move upwards with the rising
water. When the water table comes near or reaches the soil surface, appreciable upward movement of
water occurs due to evaporation from the soil surface and salts accumulate in the root zone Abrol,
(1986). Beyond the threshold level of the water table, the rate of evaporation and associated salinization
increase rapidly. The high temperature conditions often exaggerate these conditions. Different soil types
have different threshold levels, but these are commonly reached in irrigated situations. Secondary
salinization can also occur due to the use of inadequate quantities of irrigation water to leach salts that
accumulate in the root zone due to evaporation Umali, (1993). It was realized that the reaction of crops
to saline irrigation water was affected not only by the salinity level but also by soil characteristics,
irrigation practices such as the type of system and timing and the amount of irrigation applications.
Moreover, different crop varieties react differently. Whether to use irrigation water of marginal quality
would also depend on the level of yield reduction one is prepared to accept Rhoades and Loveday,
(1990). For conventional surface irrigation, and a leaching fraction of 0.1 (i.e. 10% more water than is
needed to satisfy the crop evaporative demand), water salinity should not exceed 1dS m-1 for sensitive
crops. For moderately sensitive, the threshold is 1.8 dS m-1; for moderately tolerant, 3.3 dS m-1; and
for tolerant crops, 5.8 dS m-1. In each of these categories, water of higher salinity would lead to yield
decline. Higher leaching fractions move the threshold value up, but by how much, depends on the
circumstances Rhoades and Loveday, (1990). In the wheat /cotton rotation as practiced in the Sirsa
District of India with critical salt tolerance levels of 6 dS m-1 for wheat and 7.7 dS m-1 for cotton, the
leaching fraction can be as low as 5% in case of fresh groundwater (EC < 1.5 dS m-1) and should be
15% in case of moderately saline groundwater (EC = 5.0 dS m-1) Leffelaar et al., (2003). The rocks
with naturally high salt content after weathering add salinity in aquifers. Saline water is denser than
fresh water therefore, with the increasing depth generally salinity increases. However, the regions have
been observed where ground water is pumped up for irrigation salinity gradients are reversed through
local irrigation Kijne and Vander Velde (1992). Rising water tables not only induce soil secondary
salinization based on the upward movement of salts from saline aquifers and saline soils it accelerates
the water and salts into rivers water bodies, causing salinization in lowlands or in the aquifer flow
system Fig. (5).

287
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 5: Processes leading to salinization of aquifers in inland areas. After Foster and Chilton, (2003)
and Rocha et al., (2020)

The main causes of water salinization are the accelerated groundwater seepage to surface systems
and discharge of irrigation return flows. However, domestic and industrial discharges of wastewater
also contribute to surface water salinization. Intrusion of seawater into coastal aquifers also adds
salinization of groundwater resources. The over-extraction of groundwater on the one hand result into
decline of water tables and depletion of aquifers, on the other hand it results into increased salinity of
the water that remains.

3.1. Effects of salinity on plants

Soil salinity is a major factor that limits the yield of agricultural crops, jeopardizing the capacity
of agriculture to sustain the burgeoning human population increase Flowers, (2004); Munns and Tester,
(2008); Parida and Das, (2005). At low salt concentrations, yields are mildly affected or not affected at
all Maggio et al., (2001). As the concentrations increase, the yields move towards zero, since most
plants, glycophytes, including most crop plants, will not grow in high concentrations of salt and are
severely inhibited or even killed by 100-200 mM NaCl. The reason is that they have evolved under
conditions of low soil salinity and do not display salt tolerance Munns and Termaat, (1986). On the
contrary, halophytes can survive salinity in excess of 300-400 mM. Halophytes are known to have a
capability of growth on salinized soils of coastal and arid regions due to specific mechanisms of salt
tolerance developed during their phylogenetic adaptation. Depending on their salt-tolerating capacity,
these plants can be either obligate and characterized by low morphological and taxonomical diversity
with relative growth rates increasing up to 50% sea water or facultative and found in less saline habitats
along the border between saline and non-saline upland and characterized by broader physiological
diversity which enables them to cope with saline and non-saline conditions Parida and Das, (2005).
Measurements of ion contents in plants under salt stress revealed that halophytes accumulate salts
whereas glycophytes tend to exclude the salts Zhu, (2007).
Halophyte-glycophytes associations, in many arid and semi-arid regions are saline and are not
thus proper for the cultivation of traditional crops. In these soils, two major vegetation types can coexist
(i) a halophytic vegetation, naturally salt-tolerant and (ii) a glycophytic vegetation, generally salt
sensitive, but capable of growing in association with halophytes Fig. (6). The coexistence of both types
of vegetation (halophytes and glycophytes) can be explained by the stratification of root systems of
perennial halophytes, to exploit only the deepest and salty horizons, and root systems of annuals, which
thrive in the less saline surface areas Abdelly et al., (2006). Several hypotheses can explain the low
salinity of the higher horizon. The upper layer can be washed away by a lateral flow of water lightly
loaded to the center of the depression. Halophytes, by exploiting the saline deep horizons, may limit the
rise of saline groundwater to the surface allowing rainwater to penetrate the upper horizon of the profile.
Finally, the halophytes, through their shallow roots, can help maintaining low levels of salt in surface

288
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

horizon. These factors favor the rapid development of a carpet of annuals less resistant to salt stress but
very efficient in the acquisition of mineral resources as soon as the water resources permit Abdelly et
al. (2006). These data clearly show that some halophytes are capable of desalinizing and fertilizing
soils, thus creating micro- habitats favorable for the development of several salt-sensitive annual plants.
The latter are represented mainly by Medicago species that are highly preferred by livestock Abdelly et
al., (2011). Other halophytes are well grazed and contribute directly to the pastoral value of marginal
zones. Many of these species are capable of maintaining high growth potentials, under a wide range of
salinities, and in the case of the Poaceae to produce plant biomass with low salt concentrations Abdelly
et al., (2011). Such highly interesting findings, when properly and explicitly explained to farmers, may
encourage using saline soils and plants in agricultural systems. Farmers will also need to know more
about the different kinds of halophytes, their requirement, the mechanisms of their salt tolerance and
especially their potential interests.

Fig. 6: Perennial halophytes in Sabkhas favouring the growth of annuals (Leguminous, Poaceae)
through efficient salt removal from the soil, N and P fertilization. After Abdelly et al., (2006) & (2011)
and Ben Hamed et al., (2014)

High salinity affects plants in two main ways, high concentrations of salts in the soil disturb the
capacity of roots to extract water, and high concentrations of salts within the plant itself can be toxic,
resulting in an inhibition of many physiological and biochemical processes such as nutrient uptake and
assimilation Hasegawa et al., (2000), Munns, (2002); Munns et al., (1995); Munns and Tester, (2008).
Excessive amounts of salt enter the plant in the transpiration stream, there will be injury to cells in the
transpiring leaves and this may cause further reductions in growth. This is called the salt specific or ion-
excess effect of salinity Greenway and Munns, (1980). These salinity effects has threefold effects viz.
it reduces water potential and causes ion imbalance or disturbances in ion homeostasis and toxicity; this
altered water status leads to initial growth reduction and limitation of plant productivity. Together, these
effects reduce plant growth, development and survival. A two-phase model describing the osmotic and
ionic effects of salt stress was proposed by Munns et al., (1995) Fig (7), (8).

289
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 7: Scheme of the two-phase growth response to salinity. After Munns, (1995).

Plants sensitive or tolerant to salinity differ in the rate at which salt reaches toxic levels in leaves.
Timescale is days, weeks, or months, depending on the species and the salinity level. During phase 1,
growth of both type of plants is reduced because of the osmotic effect of the saline solution outside the
roots. During phase 2, old leaves in the sensitive plant die and reduce the photosynthetic capacity of the
plant. This exerts an additional effect on growth. In the first, osmotic phase, which starts immediately
after the salt concentration around the roots increases to a threshold level making it harder for the roots
to extract water, the rate of shoot growth falls significantly. An immediate response to this effect, which
also mitigates ion flux to the shoot, is stomatal closure. However, because of the water potential
difference between the atmosphere and leaf cells and the need for carbon fixation, this is an untenable
long-term strategy of tolerance Hasegawa et al., (2000). Shoot growth is more sensitive than root growth
to salt- induced osmotic stress probably because a reduction in the leaf area development relative to
root growth would decrease the water use by the plant, thus allowing it to conserve soil moisture and
prevent salt concentration in the soil Munns and Tester, 2008). A reduced leaf area and stunted shoots
Läuchli and Epstein, (1990) commonly express reduction in shoot growth due to salinity. The growth
inhibition of leaves sensitive to salt stress appears to be also a consequence of inhibition by salt of
symplastic xylem loading of Ca2+ in the root Läuchli and Grattan, (2007) Fig. (8).

Fig. 8: The three main mechanisms of Salinity tolerance in a crop plants. Tissue tolerance where high
salt concentrations are found in leaves but are compartmentalized at the cellular and intracellular level
(especially in the vacuole), a process involving ion transporters, proton pumps and synthesis of
compatible solutes. Osmotic tolerance, which is related to minimizing the effects on the reduction of
shoot growth and may be related to as yet un known sensing and signaling mechanisms. Ion exclusion,
where Na+ and Cl transport processes, predominantly in roots, prevent the accumulation of toxic

290
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

concentrations of Na+ and Cl within leaves. Mechanisms may include retrieval of Na+ from the xylem,
compartmentation of ions in vacuoles of cortical cells and/or efflux of ions back to the soil. After Pravin
et al., (2018)
Final leaf size depends on both cell division and cell elongation. Leaf initiation, which is
governed by cell division, was shown to be unaffected by salt stress in sugar beet, but leaf extension
was found to be a salt-sensitive process Papp et al., (1983), depending on Ca2+ status. Moreover, the
salt-induced inhibition of the uptake of important mineral nutrients, such as K+ and Ca2+, further reduces
root cell growth Larcher, (1980) and, in particular, compromises root tips expansion. Apical region of
roots grown under salinity show extensive vacuolization and lack of typical organization of apical
tissue. A slight plasmolysis due to a lack of continuity and adherence between cells is present with a
tendency to the arrest of growth and differentiation. Otherwise, control plants root tips characterizing
by densely packed tissues with only small intercellular spaces. The second phase, ion specific,
corresponds to the accumulation of ions, in particular Na+, in the leaf blade, where Na+ accumulates
after being deposited in the transpiration stream, rather than in the roots Munns, (2002). Accumulation
of Na+ turns out to be toxic especially in old leaves, which are no longer expanding and so no longer
diluting the salt arriving in them as young growing leaves do. If the rate at which they die is greater
than the rate at which new leaves are produced, the photosynthetic capacity of the plant will no longer
be able to supply the carbohydrate requirement of the young leaves, which further reduces their growth
rate Munns and Tester, (2008). Abiotic stresses including salinity have been widely shown to severely
impact all the phases of photosynthesis, the most fundamental and intricate physiological process in
plants Jahan et al., (2020); Sehar et al., (2021);Ghanem et al., (2021). In fact, the overall status of
photosynthesis can be due to stress-induced change in its various components including photosynthetic
pigments and photosystems, the electron transport system, and CO2 reduction pathways. Chlorophyll
(Chl) is among the sensitive indicators of cellular metabolic state Ghanem et al., (2021). The content
of Chl (a) and Chl (b) was significantly reduced under salinity in cucumber seedlings Fatma et al.,
(2021). The photosynthetic pigments as Chl (a) and Chl (b), carotenoids and net photosynthesis rate
along with stomatal conductance were highly affected by the salt concentration in watermelon plants
Li et al., (2017). In another study, 100 mM NaCl-mediated reduction of Chl (a) and Chl (b) and
carotenoids contents was shown in rice Mahdieh et al., (2015). In salinity exposed T. aestivum, a greater
decline in the photosynthetic rate and electron transport rate and saturating photosynthetically active
photo flux density was noted Sehar et al., (2021). Moreover, there were reductions in the number of
photosynthetic pigments such as Chl and carotenoids with the net photosynthesis, stomatal conductance,
intercellular CO2 concentration, and transpiration rate under stress in tomato plants Jiang et al., (2017).
The photosystem II (PS II) is the prime site affected by any change in electron transport chain activity
due to stress such as salinity Jiang et al., (2017) Fig (9).

Fig. 9: Illustrates the photosystem II (PS II) affected by abiotic stresses including salinity have been
severely impact all the phases of photosynthesis

291
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Severe reduction in the efficiency of PS II, the electron transport system, and the CO2 assimilation
rate under salinity stress has been reported Sehar et al., (2021). Decreased growth was obtained in barley
plants due to salt-accrued damaged Chl fluorescence and oxygen evolving complex Kalaji et al., (2011).
It has been observed that growth becomes reduced in plants due to damage of PS II and electron
transport rates under stress Fatma et al., (2021). In B. juncea, the increased concentration of salt
significantly affected net photosynthetic rate, stomatal conductance, intercellular CO2, quantum yield
of PS II, Rubisco activity, and PNUE Jahan et al., (2021). The study of Singh et al. Singh et al., (2016)
showed the response towards variable concentration of salt, which hampered the photosynthetic
apparatus and the water splitting efficiency complex. The photosynthetic pigment content and plant
growth were greatly reduced under salinity stress in salt-sensitive Sorghum plants Nxele et al., (2017).
Salt stress was also reported to cause reductions in leaf area, pigment content, Hill reaction, 14CO2
fixation, and morphology of chloroplasts, number of reaction centers, net CO2 assimilation rate, and
Rubisco activity in wheat Aldesuquy et al., (2014). Salinity-mediated down regulation of
photosynthetic gas exchange rate, water utilization efficiency was reported to lead to reductions in
quantum yield of PS II, photochemistry, and photochemical quenching Wu et al., (2012). Hussain et
al., (2019) showed that salt stress reduced net photosynthetic rate, and intercellular CO2 concentration
in rice. In photosynthetic tissues, in fact, Na+ accumulation affects photosynthetic components such as
enzymes, chlorophylls, and carotenoids Davenport, et al., (2005); El-Sebai et al., (2016). In addition,
Abdallah et al., (2016) noticed that, the rice varieties Giza 178 showed a more pronounced increased in
photosynthetic pigments as compared with Giza 177 from the previous observations Giza 177 was
considered less tolerant to salinity than Giza 178. The inhibitory effect of salinity stress on the
photosynthetic pigments may be due to the effect of salinity on the activities of photosynthetic enzymes
and this may be a secondary effect mediated by the reduced CO2 partial pressure in the leaves caused
by stomatal closure. The derived reduction in photosynthetic rate in the salt sensitive plants can increase
also the production of reactive oxygen species (ROS). Dolatabadian and Saleh Jouneghani, (2009)
found that, salinity stress leads to an increase in free radicals in chloroplasts and destruction of
chlorophyll molecules by ROS, which results in reduction of photosynthesis and growth of common
bean.
Normally, antioxidative mechanisms, but salt stress Allan and Fluhr, (1997) rapidly remove ROS;
Foyer and Noctor, (2003), can impair this removal. ROS signalling has been shown to be an integral
part of acclimation response to salinity. ROS play, in fact, a dual role in the response of plants to abiotic
stresses functioning as toxic by-products of stress metabolism, as well as important signal transduction
molecules integrated in the networks of stress response pathway mediated by calcium, hormone and
protein phosphorylation Miller et al., (2010). ABA plays an important role in the response of plants to
salinity and ABA-deficient mutants perform poorly under salinity stress Xiong et al., (2001). Salt stress
signalling through Ca2+ and ABA mediate the expression of the late embryogenesis–abundant (LEA)-
type genes including the dehydration-responsive element (DRE)/C-repeat (CRT) class of stress-
responsive genes Cor. The activation of LEA-type genes may actually represent damage repair
pathways Xiong et al., (2002). Both ABA dependent and independent signalling pathways mediate salt
and osmotic stress regulation of Lea gene expression. Both the pathways use Ca2+ signalling to induce
LEA- gene expression during salinity. It has been shown that ABA-dependent and - independent
transcription factors may cross talk to each other in a synergistic way to amplify the response and
improve stress tolerance Shinozaki and Yamaguchi-Shinozaki, (2000)

3.2. Germination
The abiotic stress is known as salinity all over the world and especially in arid and semi-arid
areas harms plant growth and yields Abbasi et al., (2016); Rani et al., (2019). According to Okorogbona
et al., (2018), these elements mark nearly one-third of the world’s irrigated land. When a plant is
exposed to a salt stress condition, this factor disturbs the normal metabolism of the plant; as a result,
the plant’s growth and its productivity are reduced (Abbasi et al., 2014). When seeds are sown in a
saline environment, these seeds with low osmotic-potential don’t absorb water in a saline medium,
accumulation process of different toxic ions (such as Na+ and Cl- ) increases, finally, the process of
seed-germination first delayed, reduced, and disrupted. This feature also triggered a negative impression
on the germination process, its percentage, and seedling-growth Agnihotri et al., (2006). Seed
germination is one of the most fundamental and vital phases in the growth cycle of a plant that

292
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

determines the yield. However, it has been established that salinity adversely affects the process of
germination in various plants like Posidonia Fernández-Torquemada and Sánchez-Lizaso, (2013),
Oryza sativa (Xu et al., 2011), Triticum aestivum Akbarimoghaddam et al. (2011), Zea mays Carpıcı
et al. (2009); Khodarahmpour et al., (2012), and Brassica spp. Ibrar et al., (2003); Ulfat et al., (2007).
Salinity affects the germination process many-folds. It alters the imbibition’s of water by seeds due to
lower osmotic potential of germination media Khan and Weber, (2008) causes toxicity which changes
the activities of enzymes of nucleic acid metabolism Gomes-Filho et al. (2008), alters protein
metabolism Dantas et al., (2007), disturbs hormonal balance Khan and Rizvi, (1994) and reduces the
utilization of seed reserves Othman et al., (2006). The germination rates and percentage of germinated
seeds at a particular time vary considerably among species and cultivars Fig. (10). Lauchli and Grattan,
(2007) proposed a generalized relationship between percent germination and time after adding water at
different salt levels. Kaveh et al., (2011) found a significant negative correlation between salinity and
the rate and percentage of germination that resulted in delayed germination and reduced germination
percentage in Solanum lycopersicum.

Fig. 10: Schematic representation of the seed imbibition process occurring under physiological
conditions (water) and in the presence of osmotic stress (water? osmotic agent). A Reactive oxygen
species (ROS) accumulation, which is concomitant with water intake, causes oxidative DNA damage
within embryo cells and the consequent activation of DNA repair mechanisms. The gene functions and
the related DNA repair pathways, already demonstrated to be upregulated during seed imbibition, are
listed. B When seed imbibition is carried out in the presence of an osmotic agent, the rate of water
uptake is reduced and the level of oxidative DNA damage strongly increases. In this case, changes are
observed in the expression profiles of DNA repair genes, since their up-regulation is temporally
delayed. At Arabidopsis thaliana, Mt Medicago truncatula, DSBR double strand break repair, BER base
excision repair, NER–GGR nucleotide excision repair–global genome repair, NER–TCR nucleotide
excision repair–transcription coupled repair, PARP poly(ADP-ribose)polymerase, Tdp tyrosyl-DNA
phosphodiesterase, TFIIS transcription elongation factor II-S, Top1 DNA topoisomerase I. After
Balestrazzi et al., (2011)

Bordi, (2010) reported that the germination percentage in Brassica napus significantly reduced at
150 and 200 mM NaCl. Germination rate also decreased on increasing concentration of salinity levels.
Compared with control, germination percentage, and germination speed were decreased by 38 and 33,
respectively, at 200 mM NaCl. In a recent study, Khodarahmpour et al. (2012) observed drastic
reduction in germination rate (32 %), length of radicle (80 %) and plumule (78 %), seedling length (78),
and seed vigor (95 %) in Z. mays seeds exposed to 240 mM NaCl Fig.(11).

293
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 11: Illustrates the effect of KCl, KNO3, and CaCl2 seed priming on the final germination rate
(FG%) of two b barley species, Hordeum maritimum and Hordeum vulgare (L. Manel), subjected to
various salt concentrations species, Hordeum maritimum and Hordeum vulgare (L. Manel), subjected
to various salt concentrations (0, 100, and 200 mM NaCl) for 7 days at the germination stage. Values
are means of 20 replicates _ standard error. Data with the same letter are not significantly different at p
< 0.05 (Duncan’s test). Ben Youssef et al., (2021).

3.3. Growth
One of the initial effects of salt stress is the reduction of growth rate. Salt in soil water inhibits
plant growth for two reasons. First, it reduces the plant’s ability to take up water and this leads to slower
growth. This is the osmotic or water deficit effect of salinity. Second, it may enter the transpiration
stream and eventually injure cells in the transpiring leaves, further reducing growth Fig. (12). Zorb et
al., (2019) stated that Na+ and Cl- at high amounts are toxic to plants, especially if they increase in the
cytosol. Despite this relevance, not much is known about cytosolic processes that are impaired by
excessive concentrations of salt ions. For instance, toxicity effects of chloride in the cytosol remain to
be elucidated Geilfus, (2018a). Plants that are exposed to excessive concentrations of salt ions are
poisoned and eventually die. The ion-toxicities have diverse consequences resulting in ionic imbalance
i.e. in terms of uptake competition of Na+ with K+ , Ca2+ and Mg2+ and may accelerate senescence of
transpiring leaves, not only because of toxic concentrations of deleterious ions in photosynthetic active
tissues but also reduced availability of the beneficial nutrients. The energy gain of a crop under salinity
stress is schematized in Fig. 12. At any given time, a finite amount of energy and resources that can be
harvested by the plant through photosynthesis or metabolically utilized Munns and Gilliham, (2015).
Under non-stressed conditions, plants use the majority of the energy in processes necessary for
maintenance and vegetative and generative growth. However, resource allocation changes with
increasing levels of salinity as increasing resources are invested in the mitigation of stress Fig. (12). the
majority of vegetable crops have a very low salinity threshold that is 2.5 dS m-1 Snapp et al., (1991).
Thus, the area of soils with restrictions for vegetable crop production is therefore greater than the area
that is defined as ꞌsalinizedꞌ. Since a saline soil is generally defined as showing an EC value of the
saturation extract (ECe) in the root zone that exceeds 4 dS m-1 (approximately 40 mM NaCl) at 25 °C
and having an exchangeable Na+ level of 15% Shrivastava and Kumar, (2014). The performance of
sensitive and tolerant crops in dependence of soil salinity can be summarized in a simplified scheme as
shown in Fig. (12 B).
This is the salt-specific or ion-excess effect of salinity. The two effects give rise to a two-phase
growth response to salinity given by Munns, (1993&2005); reported that the first phase of the growth
response results from the effect of salt outside the plant. The salt in the soil solution reduces leaf growth
and to a lesser extent root growth Munns, (1993). The cellular and metabolic processes involved are in
common to drought-affected plants. Neither Na+ nor Cl− builds up in growing tissues at concentrations
that inhibit growth: meristematic tissues are fed largely in the phloem from which salt is effectively
excluded, and rapidly elongating cells can accommodate the salt that arrives in the xylem within their

294
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

expanding vacuoles. Phase 2: The second phase of the growth response results from the toxic effect of
salt inside the plant. The salt taken up by the plant concentrates in old leaves: continued transport into
transpiring leaves over a long period eventually results in very high Na+ and Cl−concentrations, and the
leaves die. The cause of injury is probably the salt load exceeding the ability of cells to
compartmentalize salts in the vacuole. Salts would then build up rapidly in the cytoplasm and inhibit
enzyme activity. Alternatively, they might build up in the cell walls and dehydrate the cell.

Fig. 12: Schematic of energy gain and energy use by a crop plant and performance of crops under
salinity stress. (A) The proportion of energy used for maintenance, growth and stress defense is
portrayed. The relative proportions will change depending on the developmental stage of the plant and
exposure to salt stress–maintenance costs will be greater when plants are larger. Total energy gain will
decrease with greater salinity by decreasing photosynthetic rate following induced closure of stomata
and damage to cellular and photosynthetic machinery. Stress tolerance mechanisms represent additional
costs to the plant required to deal with the salt load in the soil (for example, but not limited to, greater
costs in ion exclusion or compartmentation, maintaining ion homeostasis and reactive oxygen species
(ROS) detoxification). At high salinity, there will be zero growth, as the total costs to the plant equal
energy gain; when costs exceed energy gained, then tissue will senesce. Source; adapted from a concept
by A. H. Millar and H. Lambers, based on data and reasoning of Van der Werfet al., (1988); Munns
and Gilliham, (2015). (B) Response of a sensitive and a tolerant crop to soil salinity. Both crop types
display response to salinity that can be grouped in phases: homeostasis maintains high growth rate,
eustress elicits defense gene expression and dysstress causes stagnation and death. The salinity range is
narrow in sensitive crops and broad in tolerant ones. The induction of defense in sensitive crops occurs
early, with less magnitude. After Zorb et al., (2019)

The excessive salt concentration correspondingly increases the osmotic potential of the soil that
restricts the water uptake by plants. The Na+ and Cl− ions are the major ions that produce many
physiological disorders and detrimental effects on plants. However, Na+ is the primary ion as it
interferes with the uptake of potassium (K+) ion and disturbs stomatal regulation that ultimately causes
water loss while the Cl− ion disturbs the chlorophyll production and causes chlorotic toxicity. Cl− is
more dangerous than Na+ Tavakkoli et al., (2011). Moreover, the need of Cl− in plant is essential as
well and is required for the regulation of turgor pressure and pH and enzyme activities in the cytoplasm.
Dang et al., (2008). Colmenero-Flores et al., (2019), stated that a recently reported and unexpected
effect of Cl− nutrition on the physiology (Photosynthesis, and Water-Use Efficiency (WUE) of tobacco
plants is the reduction of leaf transpiration because of a lower stomatal conductance (gs; Franco-
Navarro et al., 2016). This effect was not a consequence of a lower stomatal opening, but resulted from
the reduction of the stomatal density associated to the higher enlargement of leaf cells in Cl−-treated
plants Franco-Navarro et al., (2019). Therefore, Cl− simultaneously stimulates growth and reduces
water consumption, which results in a clear improvement of water-use efficiency (WUE), Franco-
Navarro et al., (2016), Franco-Navarro et al., (2019). Interestingly, the reason why a lower gs does not
result in lower photosynthetic capacity (as expected for C3 plants) is that Cl− specifically increases the
mesophyll diffusion conductance to CO2 (gm), Franco-Navarro et al., (2019). This phenomenon is
associated, at least in part, with a higher surface area of chloroplasts exposed to the intercellular airspace

295
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

of mesophyll cells, pointing to a role of Cl− nutrition on chloroplast performance. The higher gm
compensates for the reduction in gs, resulting in overall higher WUE Fig. (13). Increasing crop yields,
while also improving WUE has become a major focus of plant research. The beneficial effect of
macronutrient Cl− levels in maintaining high photosynthesis rates while improving WUE is particularly
challenging in C3 plants, in which water loss through transpiration is inherent to the process of fixing
atmospheric CO2. Based on number of field trials, concluded that Cl− concentration in the soil was more
important to growth and yield reduction than Na+ and the critical level (defined as the concentration
that reduces the growth or yield by 10 %) of subsoil Cl− concentration was estimated to be 490 mg. Cl−
.kg−1 soil. The Cl− concentration in the youngest mature leaf of bread wheat, durum wheat, and chickpea
showed greater variability with increasing levels of subsoil constraints than Na+ concentration Dang et
al. (2006). However, it is toxic to plants at high concentrations with critical levels for toxicity reported
to be 4–7 mg. g−1 Cl−- sensitive species and 15–50 mg. g−1 Cl−, tolerant species, Xu et al., (2000); White
and Broadley, (2001).

Fig. 13: Chloride (Cl−) nutrition at macronutrient levels significantly increases the size of leaf cells,
resulting in a reduction in stomatal density and, therefore, conductance (gs). At the same time, Cl−
improves mesophyll diffusion conductance to CO2 (gm), due, at least in part, to increased surface area
of chloroplasts exposed to the intercellular airspace. The higher mesophyll diffusion conductance
compensates for the reduction in stomatal conductance, resulting in overall higher WUE Franco-
Navarro et al., (2019). Upward arrows indicate higher values, and downwards indicate lower values.
Maron, 2019. After Colmenero-Flores et al., (2019).

3.4. Yield
Effects of salt stress on plants ultimately lead to reduction of yield production that is the most
countable effect of salt stress in agriculture. Different yield components of Vigna radiate were
significantly affected by salinity stress as reported by Nahar and Hasanuzzaman, (2009) Fig. (14). Nahar
and Hasanuzzaman, (2009) reported that numbers of pods per plant, seeds per pod, and seed weight
were negatively correlated with salinity levels. The reproductive growth of V. radiata was also affected
by salinity as the number of pods per plant substantially decreased with increasing salinity levels.
Application of 250 mM NaCl gradually reduced the yield production by about 77, 73, and 66 % V.
radiata cv. BARI mung-2, BARI mung-5, and BARI mung-6, respectively as compared to the untreated
one. The reduction of yield production may be attributed to low production, expansion, senescence, and
physiologically less active green foliage under salt stress Wahid et al., (1997), and thus, reduced
photosynthetic rate might be a supplementary effect Seemann and Critchley, (1985); Sadak et al.,
(2012).

296
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 14: Relative yield in response to different salinity levels and varying degree of salt tolerance. After
Mass, (1986) and Hasanuzzaman et al., (2013)

Hasanuzzaman et al., (2009) stated that in O. sativa varieties, grain yield, which is the ultimate
product of yield components, is greatly influenced by salinity levels. The loss of grain yield due to
150mM salinity was 50, 38, 44, and 36% over control for the cultivars BR11, BRRI dhan41, BRRI
dhan44, and BRRIdhan46, respectively. The severe inhibitory effects of salts on fertility may be due to
differential competition in carbohydrate supply between vegetative growth and constrained supply of
these to the developing panicles (Murty and Murty, (1982). In addition, reduced viability of pollen
under stress condition could result in failure of seed set Abdullah et al., (2001). Linghe and Shannon,
(2000) and Gain et al., (2004) also report grain yield reduction of rice varieties due to salt stress earlier.
Greenway and Munns, (1980) reported that, application of 200 mM NaCl, a salt-tolerant species such
as sugar beet might have a reduction of only 20 % in dry weight, a moderately tolerant species such as
cotton might have a 60 % reduction, and a sensitive species such as soybean might be dead. On the
other hand, a halophyte such as Suaeda maritima might be growing at its optimum rate Flowers et al.,
(1986). Semiz et al., (2 012) stated that increasing irrigation with saline water particularly in F. vulgare,
gradually decrease the yields and plant growth parameters such as plant height, fresh weight yield, and
biomass.

3.5. Salinity and ionic toxicity

The presence of excessive soluble salts in the soil competes with the uptake and metabolism of
mineral nutrient that are essential to plants. The appropriate ion ratios provide a tool to the physiological
response of a plant in relation to its growth and development Wang et al., (2003). However, increased
salt uptake induces specific ion toxicities like that of high Na+, Cl−, or sulfate (SO4 2−) that decrease the
uptake of essential nutrients like phosphorus (P), potassium (K+), nitrogen (N), and calcium (Ca++; Zhu,
(2001); El-Sebai, et al., (2016) Fig. (15).

297
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 15: The schematic presentation of a plant cell includes three compartments that are defined by the
extracellular space; cytosolic space and vacoula rspace. Indicated are the osmolytes and ions
compartmentalized in the cytoplasm and vacuole, and transport proteins responsible for Na+ and Cl−
homeostasis across the plasma membrane and tonoplast. Included are organelles (chloroplast (chlcp),
mitochondrion (mitmt), and peroxisome (perox) for which the importance of ROS-scavenging is
implicated. After Parihar et al., (2015)

Salinity enhances the Na+ content in Vicia faba while the Na+/K+ ratio was decreased Gadallah,
(1999) thus suggesting a negative relationship between Na+ and K+. In addition, many of the deleterious
effects of Na+ seem to be related to the structural and functional integrity of membranes Kurth et al.,
(1986). Salinity stress causes an increase in the levels of Na+ and Cl− in Atriplex griffithii in root, stem,
as well as in leaves, and the highest ion accumulation was found in leaves followed by stem and root
suggesting a positive relationship between Na+ and Cl− concentration. The Ca2+ content was reduced in
shoots and leaves of A. griffithii plants grown at high salinity; however, being stable in roots and the
K+ content was reduced with increased levels of salinity, particularly in leaves. On the other hand, Mg2+
concentration was not much affected in stems and roots but the decrease in leaf was more prominent
Khan et al., (2000). Decrease in Ca2+ and Mg2+ content of leaves upon salinity stress suggests increased
membrane stability and decreased chlorophyll content, respectively Parida et al. (2004). Despite the
fact that most plants accumulate both Na+ and Cl− ions in high concentrations in their shoot tissues when
grown in saline soils, Cl− toxicity is also an important cause of growth reduction. Tavakkoli et al.,
(2011) studied the extent to which specific ion toxicity of Na+ and Cl− reduces the growth of four barley
genotypes grown in saline soils under varying salinity treatments. High Na+, Cl−, and NaCl separately
reduced the growth of barley; however, the reductions in growth and photosynthesis were greatest under
NaCl stress and were mainly additives of the effects of Na+ and Cl− stress. They also reported that Na+
and Cl− exclusion among barley genotypes are independent mechanisms and different genotypes
expressed different combinations of the two mechanisms. High concentrations of Na+ reduced K+ and
Ca2+ uptake and reduced photosynthesis mainly by reducing stomatal conductance, while high Cl−
concentration reduced the photosynthetic capacity due to non-stomatal effects and chlorophyll
degradation Tavakkoli et al., (2011). There is abundant literature indicating that plants are particularly
susceptible to salinity during the seedling and early vegetative growth stage. One of the studies in O.
sativa showed a remarkable reduction in plant height and tiller number and leaf area index in plants
grown in saline soil Hasanuzzaman et al., (2009). In Suaeda salsa, plant height, number of branches,
length of branches, and diameter of shoot were significantly affected by salt stress that was due to the
increased content of Na+ and Cl− Guan et al., (2011). While studying with Glycine max, Dolatabadian
et al., (2011) observed that salinity stress significantly decreased shoot and root weight, total biomass,
plant height, and leaf number. In one of the recent studies on Foeniculum vulgare, it has been shown
that yields and plant growth parameters including plant height, fresh weight, yield, and biomass were
affected significantly by irrigation water salinities at 0.01 probability levels Semiz et al., (2012).
However, there are many mechanisms that plants employ to combat the salt stress, retain homoeostasis,
and overcome ion toxicity Zhu, (2001); Parida et al., (2005). Some of these mechanisms include

298
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

restriction of the mechanisms involved in salt uptake, control of long distance transport of salt,
compartmentalization of salt, extrusion of salt from the plant, and prioritization of the maintenance of
K+/Na+ ratio in the cytosol.

3.6. Photosynthetic pigments and photosynthesis

Photosynthesis is one of the most important biochemical pathways by which plants convert solar
energy into chemical energy and grow. The reduction in photosynthetic rates in plants under salt stress
is mainly due to the reduction in water potential. Photosynthesis is also inhibited when high
concentrations of Na+ and/or Cl− are accumulated in the chloroplasts and chlorophyll being important
content of photosynthesis directly correlates to the healthiness of plant Zhang et al., (2005) Fig. (16).

Fig. 16: Schematic representation of the photosynthesis performance under abiotic stresses (heat,
drought, and salinity). Drought and heat stress down-regulate enzymatic activity and electron transport
chain (ETC) and cause membrane rupture, low CO2 solubility, leaf senescence, and reactive oxygen
species (ROS) production. On the other hand, salinity causes ion toxicity, membrane disruption,
reduced stomatal conductance, lower quantum yield of PSII, slow electron transport, and reduced
activity of photosynthesis related enzymes. After Muhammad et al., (2021)

Muhammad et al., (2021), stated that Salt Stress Markedly Affects Photosynthesis. Excess of salt
or saline soil substantially alters biochemical and physiological processes, especially during
photosynthesis, causing stunted plant growth, and poor productivity. Gururani et al., (2015); Ahmad et
al., (2018); Sharma et al., (2020) reported that Salt stress decrease the crop productivity by about 50%.
Moreover, salinity-induced osmotic stress reduces photosynthesis via the ionic effect on the structure
of subcellular organelles and the inhibition of metabolic processes Lawlor, (2009); Sade et al., (2010);
Ahmad et al., (2020). The cellular membranes exhibit stress responses Ashraf and Ali, (2008); Tayefi-
Nasrabadi et al., (2011), high concentration of ions, such as sodium (Na+) and chloride (Cl−) ions, in
chloroplasts causes significant damage to the thylakoid membrane Wu and Zou, (2009); Omoto et al.,
(2010). Furthermore, inorganic salts at high concentrations can cause irrecoverable inactivation of
photophosphorylation and obstruction of electron transport in the thylakoid membrane Veiga et al.,
(2007), Mittal et al., (2012). Previously, several studies showed that severe salt stress breaks down Chl,
and the excess sodium ions Na+ effect electron transport and destabilize photosynthetic activity
Pinheiro et al., (2008); Li et al., (2010). A reduction in photosynthetic pigments under salt stress was
reported in several plant species such as wheat (Arfan et al., (2007); Perveen et al., (2010), alfalfa
(Medicago sativa) Winicov and Seemann, (1990), castor bean (Ricinus communis) (Pinheiro et al.,
(2008), and sunflower (Helianthus annuus) Ashraf and Sultana, (2000); Akram and Ashraf, (2011).
Najafpour et al. (2015) reported that the high Na+ ion concentration in cells alters the potassium ion
(K+): Na+ ratio, which instantaneously affects the bioenergetics processes of photosynthesis
(degradation of photosynthetic pigments) in cyanobacteria as well as in plants Najafpour et al., (2015).
Similarly, Eckardt, (2009) showed that salt-induced alterations impair the biosynthesis and accelerate

299
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

the degradation of photosynthetic pigments Eckardt, (2009). Other studies further summarized the
reduction of Chl a and Chl b contents under salt stress in field crops, such as Paspalum vaginatum
Ivanov and Velitchkova, (2014), Centaurium erythraea Sundby and Andersson, (1985), common bean
(Phaseolus vulgaris) Sundby and Andersson, (1985), Catharanthus roseus, cowpea (Vigna
unguiculata) Taffouo et al., (2010), and Vigna subterranean Muranaka et al., (2002). Additionally,
under salt stress, the Chl precursors, glutamate, and 5-aminolaevulinic acid (ALA), remarkably affect
the biosynthesis of Chl in sunflower callus and plants Vieira Santos et al., (2001); Santos, (2004). Salt
tolerance plant species show an increase in Chl content, when grown under saline conditions Khan et
al., (2009); Akram and Ashraf, (2011), This lead to the concept that salt tolerant plant species with high
Chl content exhibit greater membrane stability and higher Chl pigment content. So far, several salt
tolerant plant species such as pea (Pisum sativum) Noreen et al., (2010), melon (Cucumis melo) Romero
et al., (1997), sunflower Akram and Ashraf, (2011), wheat Raza et al., (2006); Arfan et al., (2007),
alfalfa Monirifar and Barghi, (2009), and proso millet (Panicum miliaceum) Sabir et al., (2009) have
been screened for their salt tolerance capacity. In contradiction to the aforementioned salt screening
strategy, Juan et al. (2005) observed weak linkage between leaf Na+ level and photosynthetic pigment
content in tomato (Solanum lycopersicum) plants, indicating that chlorophyll content assimilation is not
always associated with salt tolerance, but is an indicator of saline conditions, depending on the plant
species Juan et al., (2005). A recent study revealed that salt stress (7–8 dS. m−1) is also responsible for
the reduction in the amount of carotenoids and Chl in sugarcane (Saccharum officinarum L.) plants at
different growth stages Gomathi and Rakkiyapan, (2011). Another study in hot pepper (Capsicum
annuum L.) showed a significant increase in Chl and carotenoid contents in the presence of 60 mM salt
Ziaf et al., (2009). Therefore, we speculate that the carotenoid content of plants under salt stress could
be a useful selection criterion. Additionally, salt tolerance at gene level has great potential; for example,
the rice (Oryza sativa L.) OsSUV3 gene, which encodes the Ski2 family of DExH/D-box helicases,
functions under salt stress to facilitate photosynthetic processes and assist the antioxidant machinery
Tutej et al., (2014). Together, the studies described above prove that Chl content, photosynthetic
pigments, membrane damage, and biochemical changes are of the primary targets under salt stress,
where membrane instability and pigment degradation severely affect the growth, development, and
physiological parameters of plants.
Decreasing in chlorophyll content under salt stress is a commonly reported phenomenon, and in
various studies, chlorophyll concentration has been used as a sensitive indicator of the cellular
metabolic state Chutipaijit et al., (2011). In O. sativa leaves, the reduction of chlorophyll a and b
contents of leaves was observed after NaCl treatment (200 mM NaCl, 14 days) where chlorophyll b
content of leaves (41 %) was affected more than the chlorophyll a content (33 %) Amirjani, (2011). In
another study, O. sativa exposed to 100 mM NaCl showed 30, 45, and 36 % reduction in chlorophyll a,
chlorophyll b, and carotenoids contents as compared to the control Chutipaijit et al. (2011). Saha et al.,
(2010) observed a linear decrease in the levels of total chlorophyll, chlorophyll a, chlorophyll b,
carotenoids, and xanthophylls as well as the intensity of chlorophyll fluorescence in Vigna radiata
under increasing concentrations of NaCl treatments. Compared to control, the pigment contents
decreased on an average by 31 % for total chlorophyll, 22 % for chlorophyll a, 45 % for chlorophyll b,
14 % for carotene, and 19 % for xanthophylls Saha et al., (2010). In one of the studies in cucumber, it
has been shown that total leaf chlorophyll contents significantly decreased with an increasing NaCl
levels. The decrease in total chlorophyll contents was 12, 21, and 30%at 2 and 3, and 5 dS m−1 of salt
stress, respectively, compared to non-treated plants Khan et al., (2013). Associated with the decline in
pigment levels, there was an average 16% loss of the intensity of chlorophyll fluorescence as well.
Usually, there is dominance of chlorophyll “a” over chlorophyll “b” in plants but their values become
closer with increasing salinity Mane et al., (2010). The decrease in chlorophyll content under stress is
a commonly reported phenomenon, and in various studies, this may be due to different reasons, one of
them is related to membrane deterioration Mane et al., (2010). Photosystem II (PS II) is a relatively
sensitive component of the photosynthetic system with respect to salt stress Allakhverdiev et al., (2000).
A considerable decrease in the efficiency of PS II, electron transport chain (ETC), and assimilation rate
of CO2 under the influence of salinity has been noticed Piotr and Grazyna, (2005). Demetriou et al.,
(2007) noticed alterations in photosynthetic characteristics of Scenedesmus oblique’s that result into
declined biomass accumulation. In citrus, salinity stress decreased growth by reducing of net
photosynthetic rate, stomatal conductance, performance of PSII, and photosynthetic efficiency Lòpez-

300
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Climent et al., (2008). Kalaji et al., (2011) reported that salinity stress affects growth of barley by
altering chlorophyll fluorescence (PS II) and function of oxygen evolving complex. Furthermore, Mittal
et al., (2012) observed that salt stress affects growth of Brassica juncea by affecting photosynthetic (PS
II) and electron transport rates, and D1 protein. There are some other factors that reduce photosynthetic
rates under salt stress: dehydration of cell membranes that reduce their permeability to carbon dioxide,
salt toxicity, enhanced senescence, changes in enzyme activity induced by alterations in cytoplasmic
structure, and negative feedback by reduced sink activity Iyengar and Reddy, (1996). Desingh and
Kanagaraj, (2007) also, presume that salinity stress might affect the biochemistry of photosynthesis by
causing disorientation of the lamellar system of chloroplasts and loss of chloroplast integrity leading to
a decrease in the activities of photosystems. The decrease in chlorophyll content may be due to the
formation of proteolytic enzymes such as chlorophyllase that is responsible for chlorophyll degradation
Dolatabadian, and Jouneghani, (2009). They also added that, an increase in ROS generation due to
abiotic stress such as salt stress would result in further damage to PSII and/or cause serious damage to
organelles such as chloroplast, mitochondria and plasma membrane.

3.7. Water relation

Water potential is an important physiological parameter for determining the water status of the
plants Parida and Das, (2005). According to Romero-Aranda et al., (2001) an increase of salt in the root
medium can lead to a decrease in leaf water potential and, hence, may affect many plant processes. At
very low soil water potentials, this condition interferes with plant’s ability to extract water from the soil
and maintain turgor. However, at low or moderate salt concentration (higher soil water potential), plants
adjust osmotically (accumulate solutes) and maintain a potential gradient for the influx of water. In one
of the experiments in Cucumis sativa, it has been shown that the water potential decreases linearly with
increasing salinity levels Khan et al., (2013) Fig. (17).

Fig. 17: Illustrates the effect of salinity stress on root growth, ionic homeostasis, physiological,
biochemical, and molecular processes. After Singha et al., (2021).

3.8. Nutrient imbalance

Crop performance may be adversely affected by salinity-induced nutritional disorders. However,
the relations between salinity and mineral nutrition of crops are very complex Grattan and Grieve
,(1999). The nutritional disorders may result from the effect of salinity on nutrient availability,
competitive uptake, transport, or distribution within the plant Fig. (18). Numerous reports indicated that
salinity reduces nutrient uptake and accumulation of nutrients into the plants Rogers et al., (2003), Hu
and Schmidhalter, (2005). The availability of micronutrients in saline soils is dependent on the solubility

301
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

of micronutrients, the pH of soil solution, redox potential of the soil solution, and the nature of binding
sites on the organic and inorganic particle surfaces.

Fig. 18: Diagram represents the mode of actions of biostimulants that induce the natural processes in
crops for enhancing nutrient uptake, nutrient use efficiency (NUE), resistance to abiotic stress (salinity
stress) and quality traits, as well as increasing the presence of nutrients in t soil rhizosphere.

In addition, salinity can differently affect the micronutrient concentrations in plants depending
upon crop species and salinity levels Oertli, (1991).Micronutrient deficiencies are very common under
salt stress because of high pH Zhu et al., (2004). Numerous plant studies have demonstrated that salinity
could reduce nitrogen accumulation in plants. Decreased N uptake under saline conditions occurs due
to interaction between Na+ and NH4+ and /or between Cl− and NO3− that ultimately reduce the growth
and yield of the crop Rozeff, (1995). This reduction in NO3 − uptake is associated with Cl− antagonism
Bar et al., (1997) or reduced water uptake under saline conditions Lea-Cox and Syvertsen, (1993). The
availability of phosphorous is also reduced in saline soil due to (a) ionic strength effects that reduced
the activity of PO4 3−, (b) phosphate concentrations in soil solution was tightly controlled by sorption
processes, and (c) low solubility of Ca-P minerals. Hence, it is noteworthy that phosphate concentration
in agronomic crops decreases as salinity increases Qadir and Schubert, (2002). Sodium concentration
in plant tissues increases in the high NaCl treatment and Leaf Ca2+, K+, and N decreases Tuna et al.,
(2007). Elevated sodium chloride (NaCl) levels in the root medium reduce the nutrient assimilation,
especially of K and Ca, resulting in ion imbalances of K, Ca, and Mg Keutgen and Pawelzik, (2009).
In a recent study, it has been reported that Ca2+ and Mg2+ concentrations of all plant organs transiently
declined in response to external NaCl salinity Hussin et al. (2013). The reduction in Ca2+ and Mg2+
uptake under salt stress conditions might be due to the suppressive effect of Na+ and K+ on these cations
or due to reduced transport of Ca2+ and Mg2+ ions. In addition, salinity has an antagonistic effect on the
uptake of Ca and Mg which caused by displacing Ca in membranes of root cells Asik et al., (2009) on
wheat.

3.9. Salinity and oxidative stress

Besides direct impact of salinity on plants, a common consequence of salinity is induction of
excessive accumulation of reactive oxygen species (ROS) which can cause peroxidation of lipids,
oxidation of protein, inactivation of enzymes, DNA damage, and/or interact with other vital constituents

302
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

of plant cells. Salt stress can lead to stomatal closure, which reduces carbon dioxide availability in the
leaves and inhibits carbon fixation, exposing chloroplasts to excessive excitation energy which in turn
increase the generation of ROS such as superoxide (O2 •–), hydrogen peroxide (H2O2), hydroxyl radical
(OH•), and singlet oxygen (1O2; Parida and Das, (2005); Ahmad and Sharma, (2008); Ahmad et al.,
(2010a&2011) Fig. (19). On the other hand, as salt stress is complex and imposes a water deficit because
of osmotic effects on a wide variety of metabolic activities Greenway and Munns, (1980); Cheeseman,
(1988). This water deficit leads to the formation of ROS Sairam, Tyagi, (2004). ROS are highly reactive
and may cause cellular damage through oxidation of lipids, proteins, and nucleic acids Apel and Hirt,
(2004); Ahmad et al., (2010a, b). In many plant studies, it was observed that production of ROS is
increased under saline conditions and ROS-mediated membrane damage has been demonstrated to be
a major cause of the cellular toxicity by salinity in different crop plants such as rice, tomato, citrus, pea,
and mustard Gueta-Dahan et al., (1997); Dionisio-Sese and Tobita, (1998); Mittova et al., (2004);
Ahmad et al., (2009), (2010b).

Fig. 19: Reactive oxygen species (ROS) generation process and localization in plant cells. In different
cell organelles, ROS are produced through metabolic reactions where different enzymatic and non-
enzymatic pathways are involved. ROS—reactive oxygen species; H2O2-hydrogen peroxide; 1O2-
singlet oxygen; ETC-electron transport chain; •OH—hydroxyl radical; 3Chl -triplet chlorophyll; PS I-
photosystem I; PS II-photosystem II; O2 •−superoxide anion; XOD-xanthine oxidase; SOD- superoxide
dismutase; NADPH-Nicotinamide adenine dinucleotide phosphate; UO-urate oxidase. After
Hasanuzzaman et al., (2021)

Hasanuzzaman et al., (2021) reported that sthe generation of oxygen radicals and their
derivatives, known as reactive oxygen species, (ROS) is a part of the signaling process in higher plants
at lower concentrations, but at higher concentrations, those ROS cause oxidative stress. Salinity-
induced osmotic stress and ionic stress trigger the overproduction of ROS and, ultimately, result in
oxidative damage to cell organelles and membrane components, and at severe levels, they cause cell
and plant death. The antioxidant defense system protects the plant from salt-induced oxidative damage
by detoxifying the ROS and by maintaining the balance of ROS generation under salt stress. Different

303
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

plant hormones and genes are also associated with the signaling and antioxidant defense system to
protect plants when they are exposed to salt stress. Salt-induced ROS overgeneration is one of the major
reasons for hampering the morpho-physiological and biochemical activities of plants that can be largely
restored through enhancing the antioxidant defense system that detoxifies ROS.
In one of the studies, it has been shown that long-term salinity treatments (EC 5.4 and 10.6 dS.
m−1, 60 days) causes significant increase in H2O2 and lipid peroxidation in wheat seedlings, which was
higher in salt-sensitive cultivar than salt tolerant cultivar Sairam et al., (2002). In a recent study,
increased lipid peroxidation and levels of H2O2 were observed with increased salinity in Brassica napus
Hasanuzzaman and Fujita, (2011a) and Triticum aestivum Hasanuzzaman and Fujita, (2011b). It has
been shown that the production of ROS during environmental stresses such as salinity is one of the main
causes for decreases in crop productivity Halliwell and Gutteridge, (1989); Asada, (1994). Therefore,
regulation of ROS is a crucial process to avoid unwanted cellular cytotoxicity and oxidative damage
Halliwell and Gutteridge (1989).

4. Salt tolerance strategies in plants

Salt tolerance is the ability of plants to grow and complete their life cycle on a substrate that
contains high concentrations of soluble salt. Plants that can survive on high concentrations of salt in the
rhizosphere and grow well are called halophytes. Depending on their salt-tolerating capacity, halophytes
are either obligate or characterized by low morphological and taxonomical diversity with relative
growth rates increasing up to 50 % seawater or facultative and found in less saline habitats along the
border between saline and non-saline upland and characterized by broader physiological diversity that
enables them to cope with saline and non-saline conditions. Salt tolerance is a complex trait involving
several interacting properties. There has been increasing interest in studying the omics tools, i.e.,
genomics, transcriptomics, proteomics, metabolomics, etc. to identify and understand salt tolerance
components and mechanisms at molecular level Inan et al., (2004) Fig.(20).

Fig. 20: Plant responses subjected to salt stress. Decreasing rates of new cell production may cause the inhibition
of growth as reported by Shabala et al., (2000). The reduction in dry weight accumulation could be attributed to
increasing stiffness of the cell wall due to altered cell wall structure induced by salinity. Salt stress in the root
zone causes the development of osmotic stress, which disrupts cell ion homeostasis by inducing both the inhibition
in uptake of essential nutrients such as K + and increased accumulation of Na + and Cl − Paranychianakis and
Chartzoulakis, (2005). Higher uptake of Na + competes with the uptake of other nutrient ions, especially K +and
causes K + deficiency which leads to lower K + /Na + ratio in plants under salt stress Kibria et al., (2017). Salt-
stressed plants also show significant changes in physiological and biochemical parameters of plants such as lower
level of leaf chlorophyll content, decrease in protein synthesis, increased ROS accumulation, enhanced
accumulation of compatible solutes such as proline, changes in antioxidant enzymatic activities. Thus, all the
morphological, physiological and biochemical changes of plants exposed to salt stress are combinedly responsible
for overall changes in plant growth and productivity. After Kibria and Anamul Hoque, (2019)

304
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

We will briefly review the roles of genomics, transcriptomics, proteomics, and metabolomics in
salt stress tolerance and their possible use in enhancing salinity tolerance in plants.

4.1. Physiological and Biochemical Mechanisms of Salt Tolerance

Plants develop various physiological and biochemical mechanisms in order to survive in soils
with high salt concentration. Several mechanisms such as, (a) ion homeostasis and
compartmentalization, (b) ion transport and uptake, (c) biosynthesis of osmoprotectants and compatible
solutes, (d) activation of antioxidant enzyme and synthesis of antioxidant compounds, (e) synthesis of
polyamines, (f) generation of nitric oxide (NO), and (g) hormone modulation.

4.2. Ion Homeostasis and Salt Tolerance.

Niu et al., (1995), Hasegawa, (2013) stated that maintaining ion homeostasis through ion uptake
and compartmentalization is not only crucial for normal plant growth but is also an essential process
for growth during salt stress. Irrespective of their nature, both glycophytes and halophytes cannot
tolerate high salt concentration in their cytoplasm. Reddy et al., (1992);Zhu, (2003) reported that excess
of salt either transported to the vacuole or sequestered in older tissues that eventually are sacrificed,
thereby protecting the plant from salinity stress. Major form of salt present in the soil is NaCl, so the
focus of research is the study about the transport mechanism of Na+ ion and its compartmentalization.
The Na+ ion that enters the cytoplasm is then transported to the vacuole via Na+/H+ antiporter. Two
types’ of H+ pumps are present in the vacuolar membrane: vacuolar type H+-ATPase (V-ATPase) and
the vacuolar pyrophosphatase (V-PPase) Dietz et al., (2001), Wang et al., (2001). Of these, V-ATPase
is the most dominant H+ pump present within the plant cell. During nonstress conditions, it plays an
important role in maintaining solute homeostasis, energizing secondary transport and facilitating vesicle
fusion. Under stressed condition, the survivability of the plant depends upon the activity of V-ATPase
Dietz et al., (2001). In a study performed by De Lourdes Oliveira Otoch et al., (2001) in hypocotyls of
Vigna unguiculata seedlings, it was observed that the activity of VATPase pump increased when
exposed to salinity stress but under similar conditions, activity of V-PPase was inhibited, whereas in
the case of halophyte Suaeda salsa, V-ATPase activity was upregulated and V-PPase played a minor
role Wang et al., (2001). Increasing evidence demonstrates the roles of a Salt Overly Sensitive (SOS)
stress-signalling pathway in ion homeostasis and salt tolerance Hasegawa et al., (2000); Sanders,
(2000). The SOS signalling pathway consists of three major proteins, SOS1, SOS2, and SOS3. SOS1,
which encodes a plasma membrane Na+/H+ antiporter, is essential in regulating Na+ efflux at cellular
level. It also facilitates long distance transport of Na+ from root to shoot. Overexpression of this protein
confers salt tolerance in plants Shi et al., (2000); Shi et al., (2002). SOS2 gene, which encodes a
serine/threonine kinase, is activated by salt stress elicited Ca+ signals. This protein consists of a well-
developed N-terminal catalytic domain and a C-terminal regulatory domain Liu et al., (2000). The third
type of protein involved in the SOS stress-signalling pathway is the SOS3 protein that is a myristoylated
Ca+ binding protein and contains a myristoylation site at its N-terminus. This site plays an essential role
in conferring salt tolerance Ishitani et al., (2000). C-terminal regulatory domain of SOS2 protein
contains a FISL motif (also known as NAF domain), which is about 21 amino acid long sequence, and
serves as a site of interaction for Ca2+ binding SOS3 protein. This interaction between SOS2 and SOS3
protein results in the activation of the kinase Guo et al., (2004). The activated kinase then
phosphorylates SOS1 protein thereby increasing its transport activity which was initially identified in
yeast Quintero et al., (2002). SOS1 protein is characterised by a long cytosolic C-terminal tail, about
700 amino acids long, comprising a putative nucleotide-binding motif and an auto inhibitory domain.
This auto inhibitory domain is the target site for SOS2 phosphorylation. Besides conferring salt
tolerance, it also regulates pH homeostasis, membrane vesicle trafficking, and vacuole functions
Quintero et al., (2002), Oh et al., (2010). Thus with the increase in the concentration of Na+ there is a
sharp increase in the intracellular Ca2+ level which in turn facilitates its binding with SOS3 protein. Ca2+
modulates intracellular Na+ homeostasis along with SOS proteins. The SOS3 protein then interacts and
activates SOS2 protein by releasing its self-inhibition. The SOS3-SOS2 complex is then loaded onto
plasma membrane where it phosphorylates SOS1. The phosphorylated SOS1 results in the increased
Na+ efflux, reducing Na+ toxicity Mart´ınez-Atienza et al., (2007). Many plants have developed an
efficient method to keep the ion concentration in the cytoplasm in a low level. Membranes along with
their associated components play an integral role in maintaining ion concentration within the cytosol

305
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

during the period of stress by regulating ion uptake and transport Sairam and Tyagi, (2004) Fig. (21).
Different carrier proteins, channel proteins, antiporters, carry out the transport phenomenon and
symporters. Maintaining cellular Na+/K+ homeostasis is pivotal for plant survival in saline
environments. Ma et al., (2012) have reported that Arabidopsis NADPH oxidases AtrbohD and AtrbohF
function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress.

Fig. 21: Schematic overview of ion transport mechanism in salt stress signalling pathway. Na ions enter
the cell through NSCCs under salt stress followed by increased cytosolic Ca2 concentration that
activates SOS pathway. The proteins involved in SOS pathway are CBL and CIPK. Calcium signalling
activates CDPKs also. NHX, V-ATPase and V-PPase are involved in Na sequestration in vacuole. K
uptake in root is occurred by mainly AKT and HAK. The candidate proteins for loading Na to the xylem
are KORC and retrieval of Na from xylem are occurred by HKT. Abbreviations: nonselective cation
channels (NSCCs), SALT OVERLY SENSITIVE (SOS), Calcineurin B-like protein (CBL), CBL-
interacting protein kinase (CIPK), Na /H exchangers (NHX), vacuolar H-ATPase (VATPase) and
vacuolar H?-PPase (V-PPase), Inward-rectifying K Channel (AKT) and High-affinity K transporter
(HAK), Outward rectifying K channels (KORC), High affinity K transporters (HKT). After Malakar
and Chattopadhyay, (2021).

Plants maintain a high level of K+ within the cytosol of about 100mM ideal for cytoplasmic
enzyme activities. Within the vacuole K+ concentration ranges between 10mM and 200mM. The
vacuole serves as the largest pool of K+ within the plant cell. K+ plays a major role in maintaining the
turgor within the cell. It is transported into the plant cell against the concentration gradient via K+
transporter and membrane channels. K+ transporters mediate high affinity K+ uptake mechanisms when
the extracellular K+ concentration is low, whereas K+ channels carry out low affinity uptake when the
extracellular K+ concentration is high. Thus, uptake mechanism is primarily determined by the
concentration of K+ available in the soil. On the other hand, a very low concentration of Na+ ion (about
1mMor less) is maintained in the cytosol. During salinity stress, due to increased concentration of Na+
in the soil, Na+ ion competes with K+ for the transporter as they both share the same transport
mechanism, thereby decreasing the uptake of K+ Munns and Testerm (2008); Sairam and Tyagi, (2004).
A large number of genes and proteins, such as HKT and NHX, encoding K+ transporters and channels
have been identified and cloned in various plant species. During salt stress, expression of some low
abundance transcripts is enhanced that are found to be involved in K+ uptake. This was observed in the
halophyte Mesembryanthemum crystallinum Yen et al., (2000). Transporters located on the plasma
membrane; belonging to the HKT (histidine kinase transporter) family, also play an essential role in
salt tolerance by regulating transportation of Na+ and K+. Class 1 HKT transporters that have been
identified in Arabidopsis protect the plant from the adverse effects of salinity by preventing excess
accumulation Na+ in leaves. Similar results were observed in the experiment that was carried out with
rice where class 1 HKT transporter removes excess Na+ from xylem, thus protecting the photosynthetic
leaf tissues from the toxic effect of Na+ Schroeder et al., (2013). Intracellular NHX proteins are Na+,

306
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

K+/H+ antiporters involved in K+ homeostasis, endosomal pH regulation, and salt tolerance. Barrag´an
et al., (2012) showed that tonoplast localized NHX proteins (NHX1 and NHX2: the two major
tonoplast-localized NHX isoforms) are essential for active K+ uptake at the tonoplast, for turgor
regulation, and for stomatal function. In fact more such NHX isoforms have been identified and their
roles I en ion (Na+, K+, H+) homeostasis established from different plant species (e.g., LeNHX3 and
LeNHX4 from tomato) ´alvez et al., (2012).

4.3. Compatible Solute Accumulation and Osmotic Protections

Compatible solutes, also known as compatible osmolytes, are a group of chemically diverse
organic compounds that are uncharged, polar, and soluble in nature and do not interfere with the cellular
metabolism even at high concentration. They mainly include proline Hoque et al., (2007), Tahir et al.,
(2012), glycine betaine Khan et al., (2000), Wang and Nii, (2000), sugar Kerepesi and Galiba, (2000),
Bohnert et al., (1995), and polyols Ford; (1984), Saxena et al., (2013). Organic osmolytes are
synthesized and accumulated in varying amounts amongst different plant species. For example,
quaternary ammonium compound beta alanine betaine’s accumulation is restricted among few members
of Plumbaginaceae Hanson et al., (1994), whereas accumulation of amino acid proline occurs in
taxonomically diverse sets of plants Saxena et al., (2013) Fig. (22).

Fig. 22: A generalized schematic presentation of salinity stress responses of plant after - Chen et al.,
(2014), Agarwal et al., (2013). Adaptation to salt stress starts from stress perception of complex stimuli.
The sensor proteins perceive signal, these stress signals triggers the downstream signaling processes
and gene activation through transcription factors. The mechanisms include cell integrity,
phytohormones, antioxidants, synthesis of osmolytes and ion homeostasis. The coordinated action leads
to re-establish the cellular homeostasis, protection of functional and structural proteins and membranes,
and ultimately the tolerance to salinity stress. After Muchate et al.,

The concentration of compatible solutes within the cell is maintained either by irreversible
synthesis of the compounds or by a combination of synthesis and degradation. The biochemical
pathways and genes involved in these processes have been thoroughly studied. As their accumulation
is proportional to the external osmolarity, the major functions of these osmolytes are to protect the
structure and to maintain osmotic balance within the cell via continuous water influx Hasegawa et al.,
(2000). Amino acids such as cysteine, arginine, and methionine, which constitute about 55% of total
free amino acids, decrease when exposed to salinity stress, whereas proline concentration rises in

307
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

response to salinity stress El-Shintinawy and. El-Shourbagy, (2001). Proline accumulation is a well-
known measure adopted for alleviation of salinity stress Saxena et al., (2013), Matysik et al., (2002),
and Ben Ahmed et al., (2010). Intracellular proline that is accumulated during salinity stress not only
provides tolerance towards stress but also serves as an organic nitrogen reserve during stress recovery.
Proline is synthesized from either glutamate or ornithine. In osmotically stressed cell, glutamate
functions as the primary precursor. The biosynthetic pathway comprises two major enzymes, pyrroline
carboxylic acid synthetase and pyrroline carboxylic acid reductase Fig. (23).

Fig. 23: Proline metabolism in plants: Proline synthesis occurs in the cytosol and chloroplast. Proline
degradation occurs in mitochondria. P5C - δ-pyrroline-5-carboxylate, P5CR - pyrroline-5-carboxylate
reductase, P5CS - pyrroline-5- carboxylate synthase, GSA - glutamic semialdehyde, PDH - Proline
dehydrogenase, OAT - Ornithine aminotransferase, KG - Ketoglutarate, ProT-Proline transporter. After
Khanna-Chopra etal., (2019)

Khanna-Chopra et al., (2019) reported that proline is an important compatible solute that exhibits
numerous roles during plant growth and development and under abiotic stresses including drought and
salinity. Proline protects plants against these stresses mainly by maintaining osmotic adjustment, ROS
scavenging, and modulating major enzymatic components of the antioxidant defense system. Proline
also stabilizes proteins and protein complexes in the chloroplast and cytosol and protects the
photosynthetic apparatus and the enzymes involved in detoxification of ROS during stress. The
enhanced rate of Pro biosynthesis in chloroplasts can contribute to the stabilization of redox balance
and maintenance of cellular homeostasis by dissipating the excess of reducing potential when electron
transport is saturated during adverse conditions. Proline catabolism in the mitochondria is connected to
oxidative respiration and provides energy for resumed growth after stress. Moreover, Pro oxidation can
regulate mitochondrial ROS levels and influence programmed cell death. Proline appears to function as
a metabolic signal that regulates metabolite pools and redox balance controls the expression of
numerous genes and influences plant growth and development.
Both these regulatory steps are used to overproduce proline in plants Oh et al., (2010). It functions
as an O2 quencher thereby revealing its antioxidant capability. This was observed in a study carried out
by Matysik et al., (2002); Ben Ahmed et al., (2010), they observed that proline supplements enhanced
salt tolerance in olive (Olea europaea) by amelioration of some antioxidative enzyme activities,
photosynthetic activity, and plant growth and the preservation of a suitable plant water status under
salinity conditions. It has been reported that proline improves salt tolerance in Nicotiana tabacum by
increasing the activity of enzymes involved in antioxidant defence system Hoque et al., (2008).
Deivanai et al. Deivanai et al., (2011) also demonstrated that rice seedlings from seeds pretreated with
1mM proline exhibited improvement in growth during salt stress. Glycine betaine is an amphoteric

308
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

quaternary ammonium compound ubiquitously found in microorganisms, higher plants and animals,
and is electrically neutral over a wide range of pH. It is highly soluble in water but also contains
nonpolar moiety constituting 3-methyl groups. Because of its unique structural features it interacts both
with hydrophobic and hydrophilic domains of the macromolecules, such as enzymes and protein
complexes. Glycine betaine is a nontoxic cellular osmolyte that raises the osmolarity of the cell during
stress period; thus, it plays an important function in stress mitigation. Glycine betaine also protects the
cell by osmotic adjustment Gadallah, (1999) stabilizes proteins Makela et al., (2000) and protects the
photosynthetic apparatus from stress damages Cha-Um and Kirdmanee, (2010)] and reduction of ROS
Ashraf and Foolad, (2007), Saxena et al., (2013). Accumulation of glycine betaine is found in a wide
variety of plants belonging to different taxonomical background. Glycine betaine is synthesized within
the cell from either choline or glycine. Synthesis of glycine betaine from choline is a 2-step reaction
involving two or more enzymes. In the first step, choline is oxidised to betaine aldehyde that is then
again oxidized in the next step to form glycine betaine. In higher plants, the first conversion is carried
out by the enzyme choline monooxygenase (CMO), whereas the next step is catalyzed by betaine
aldehyde dehydrogenase (BADH) Ahmad et al., (2013), another pathway that is observed in some
plants, mainly halophytic, demonstrated the synthesis of glycine betaine from glycine. Here glycine
betaine is synthesized by three successive N-methylation and the reactions are catalyzed by two S-
adenosyl methionine dependent methyl transferases, glycine sarcosine N-methyl transferase (GSMT),
and sarcosine dimethyl glycine N-methyl transferase (SDMT). These two enzymes have overlapping
functions as GSMT catalyzes the first and the second step while SDMT catalyzes the second and third
step Ahmad et al., (2013). Rahman et al., (2002) reported the positive effect of glycine betaine on the
ultrastructure of Oryza sativa seedlings when exposed to salt stress. Under stressed condition (150 mM
NaCl), the ultrastructure of the seedling shows several damages such as swelling of thylakoids,
disintegration of grana and intergranal lamellae, and disruption of mitochondria. However, these
damages were largely prevented when seedlings were pretreated with glycine betaine. When glycine
betaine is applied as a foliar spray in a plant subjected to stress, it led to pigment stabilization and
increase in photosynthetic rate and growth Cha-Um and Kirdmanee, (2010); Ahmad et al., (2013).
Polyols are compounds with multiple hydroxyl functional groups available for organic reactions. Sugar
alcohols are a class of polyols functioning as compatible solutes, as low molecular weight chaperones,
and as ROS scavenging compounds Ashraf and Foolad, (2007). They can be classified into two major
types, cyclic (e.g., pinitol) and acyclic (e.g., mannitol). Mannitol synthesis is induced in plants during
stressed period via action of NADPH dependent mannose-6-phosphate reductase. These compatible
solutes function as a protector or stabilizer of enzymes or membrane structures that are sensitive to
dehydration or ionically induced damage. It was found that the transformation with bacterial mltd gene
that encodes formannitol-1-phosphate dehydrogenase in both Arabidopsis and tobacco (Nicotiana
tabacum) plants confer salt tolerance, thereby maintaining normal growth and development when
subjected to high level of salt stress Binzel et al., (1988), Thomas et al., (1995). Pinitol is accumulated
within the plant cell when the plant is subjected to salinity stress. The biosynthetic pathway consists of
two major steps, methylation of myo-inositol that results in formation of an intermediate compound,
ononitol, which undergoes epimerization to form pinitol. Inositol methyl transferase enzyme encoded
by imt gene plays major role in the synthesis of pinitol. Transformation of imt gene in plants shows a
result similar to that observed in the case of mltd gene. Thus, Pinitol plays a significant role in stress
alleviation. Accumulation of polyols, either straight chain metabolites such as mannitol and sorbitol or
cyclic polyols such as myo-inositol and its methylated derivatives, is correlated with tolerance to
drought and/or salinity, based on polyol distribution in many species, including microbes, plants, and
animals Bohnert et al., (1995) Fig. (24).

309
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 24: Illustrates polyol pathway. Hyperglycaemia increases flux through the polyol pathway that
metabolises excess glucose. The consumption of nicotinamide adenine dinucleotide phosphate
(NADPH) in the initial conversion of glucose to sorbitol results in less NADPH availability for the
generation activity of glutathione reductase that maintains the adequate levels of reduced glutathione
(GSH), which is an important cellular antioxidant. The depletion of GSH may lead to increased levels
of reactive oxygen species, leading to oxidative stress. (NADPH, Nicotinamide adenine dinucleotide
phosphate (reduced form); NADP, nicotinamide adenine dinucleotide phosphate; NAD, nicotinamide
adenine dinucleotide; NADH, nicotinamide adenine dinucleotide (reduced form); GSSG, oxidized
glutathione; GSH, reduced glutathione). After Solani David Mathebula, (2018)

Solani David Mathebula, (2018) reported that in cellular glucose metabolism, a small fraction of
glucose is normally metabolized through the polyol pathway , Nishikawa et al., (2000); Gabbay, (1973);
Oates, (2002) ; Gabbay, (1975); Kinoshita, (1990); Coucha et al., (2015) and Mathebula, (2015). In
diabetes, there is an increase in the flux of glucose, and the excess glucose is metabolized in this
pathway. Two enzymes control the polyol pathway. Aldose reductase, the first enzyme, reduces glucose
into sorbitol using nicotinamide adenine dinucleotide phosphate (NADNP) as a cofactor. Sorbitol is
then oxidised or converted to fructose by sorbitol dehydrogenase, the second enzyme, with nicotinamide
adenine dinucleotide (NAD) as a cofactor Fig. (24). Under euglycaemic conditions, sorbitol level is
low, while during Hyperglycaemia, sorbitol level increases owing to the flux of glucose through the
polyol pathway. Since sorbitol is impermeable and cannot easily diffuse through cell or plasma
membranes, and there is a slow metabolism of sorbitol to fructose, it accumulates within the retinal
cells and causes osmotic damage to the retinal vascular cells, leading to DR
Accumulations of carbohydrates such as sugars (e.g., glucose, fructose, fructans, and trehalose)
and starch occur under salt stress Parida et al., (2004). The major role played by these carbohydrates in
stress mitigation involves osmoprotection, carbon storage, and scavenging of reactive oxygen species.
It was observed that salt stress increases the level of reducing sugars (sucrose and fructans) within the
cell in a number of plants belonging to different species Kerepesi and Galiba, (2000). Besides being a
carbohydrate reserve, trehalose accumulation protects organisms against several physical and chemical
stresses including salinity stress. They play an osmoprotective role in physiological responses Ahmad
et al., (2013). Sucrose content was found to increase in tomato (Solanum lycopersicum) under salinity
due to increased activity of sucrose phosphate synthase Gao et al., (1998). Sugar content, during salinity
stress, has been reported to both increase and decrease in various rice genotype Alamgir and Yousuf
Ali, (1999). In rice roots, it has been observed that starch content decreased in response to salinity while
it remained unchanged in the shoot. Decrease in starch content and increase in reducing and
nonreducing sugar content were noted in leaves of Bruguiera parviflora Parida et al., (2004).

310
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

4.4. Antioxidant Regulation of Salinity Tolerance.

Abiotic and biotic stress in living organisms, including plants, can cause overflow, deregulation,
or even disruption of electron transport chains (ETC) in chloroplasts and mitochondria. Under these
conditions molecular oxygen (O2) acts as an electron acceptor, giving rise to the accumulation of ROS.
Singlet oxygen (1O2), the hydroxyl radical (OH−), the superoxide radical (O−2), and hydrogen peroxide
(H2O2) are all strongly oxidizing compounds and therefore potentially harmful for cell integrity Gro et
al., (2013). Antioxidant metabolism, including antioxidant enzymes and nonenzymatic compounds,
play critical parts in detoxifying ROS induced by salinity stress. Salinity tolerance is positively
correlated with the activity of antioxidant enzymes, such as superoxide dismutase (SOD), catalase
(CAT), glutathione peroxidase (GPX), ascorbate peroxidase (APX), and glutathione reductase (GR)
and with the accumulation of nonenzymatic antioxidant compounds Asada, (1999); Gupta et al., (2005)
;Gill et al., (2013) and Tuteja et al., (2013) have recently reported a couple of helicase proteins (e.g.,
DESD-box helicase and OsSUV3 dual helicase) functioning in plant salinity tolerance by
improving/maintaining photosynthesis and antioxidant machinery Fig.(25).
Kim et al., (2013) showed that silicon (Si) application to rice root zone influenced the hormonal
and antioxidant responses under salinity stress. The results showed that Si treatments significantly
increased rice plant growth compared to controls under salinity stress. Si treatments reduced the sodium
accumulation resulting in low electrolytic leakage and lipid peroxidation compared to control plants
under salinity stress. Enzymatic antioxidant (catalase, peroxidase, and polyphenol oxidase) responses
were more pronounced in control plants than in Si-treated plants under salinity stress. Anthocyanin is a
flavonoid whose accumulation in plant exposed to salt stress has been largely documented.

Fig. 25: Represents different types of antioxidants and their combined mechanisms Hasanuzzaman et
al., (2020). Such as (SOD)-superoxide dismutase; (CAT)-catalase; (POX)-peroxidases; (AsA)-
ascorbate; (DHA)-Dehydroascorbate; (GSSG)-oxidized glutathione; (GSH)-reduced glutathione;
(APX)-ascorbate peroxidase; (MDHA)-monodehydroascorbate; (MDHAR)-monodehydroascorbate
reductase; (DHAR)-dehydroascorbate reductase; (GR)-glutathione reductase; (GST)- glutathione S-
transferase; (GPX)-glutathione peroxidase; (PPO)-polyphenol oxidase; (PRX)-peroxiredoxins; (TRX)-
thioredoxin; (NADPH)-nicotinamide adenine dinucleotide phosphate; (O2)-oxygen; e--electrons;
(H2O2)-hydrogen peroxide; (O2) •–-superoxide anion; R-aliphatic, aromatic or heterocyclic group; X-
sulfate, nitrite or halide group; ROOH-hydro peroxides; -(SH)-thiolate; -(SOH)-sulfenic acid. After
Mirza Hasanuzzaman et al., (2021).

Van Oosten et al., (2013) isolated the anthocyanin-impairedresponse- 1 (air1) mutant that is
unable to accumulate anthocyanins under salt stress. The air1 mutant showed a defect in anthocyanin
production in response to salt stress but not to other stresses such as high light, low phosphorous, high
temperature, or drought stress. This specificity indicated that air1 mutation did not affect anthocyanin

311
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

biosynthesis but rather its regulation in response to salt stress. The discovery and characterization of
AIR1 opens avenues to dissect the connections between abiotic stress and accumulation of antioxidants
in the form of flavonoids and anthocyanins. Ascorbate is one of the major antioxidants present within
the cell. Pea plants grown under saline (150mM NaCl) stress showed an enhancement of both APX
activity and Snitrosylated APX, as well as an increase of H2O2, NO, and S-nitrosothiol (SNO) content
that can justify the induction of the APX activity. Proteomic data have shown that APX is one of the
potential targets of PTMs mediated byNO-derived molecules Begara-Morales et al., (2014) Using
recombinant pea cytosolic APX, the impact of peroxynitrite (ONOO−) and S-nitrosoglutathione
(GSNO), which are known to mediate protein nitration and S-nitrosylation processes, respectively, was
analysed. While peroxynitrite inhibits APX activity, GSNO enhances its enzymatic activity. The results
provide new insight into the molecular mechanism of the regulation of APX, which can be both
inactivated by irreversible nitration and activated by reversible S-nitrosylation Begara-Morales et al.,
(2014). Exogenous application of ascorbate mitigates the adverse effects of salinity stress in various
plant species and promotes plant recovery from the stress Agarwal and Shaheen, (2007); Munir and
Aftab, (2011) and El-Sebai, et al., (2015) Fig.(26).

Fig. 26: Transverse sections through the median portion of the main stems of wheat plants grown for
56 days at 0.23 and 6.0 dS m−1 salt stress (×68) (a) 0.23 dS m−1 ; (b) 6.0 dS m−1 , and magnified
portionfrom transverse sections shown in (a,b) (×330); (c) 0.23 dS m−1 ; (d) 6.0 dS.m-1 After Rania et
al., (2020)

Rania et al., (2020) stated that examination of 14C fixation and its distribution in biochemical leaf
components, as well as the physiological and anatomical were conducted, using wheat plants (Triticum
aestivum L.) grown in diluted seawater at 0.2, 3.0, 6.0, and 12.0 dS m−1. Results revealed that application
of diluted seawater significantly reduced the chlorophyll content, 14C fixation (photosynthesis), plant
height, main stem diameter, total leaf area per plant, and total dry weight at particularly at 3.0, 6.0, and
12.0 dS m−1 seawater salt stress. The 14C loss was very high at 12.0 ds m−1 after 120 h. 14C in lipids
(ether extract), significant changes at 12.0 dS m−1 at 96 and 120 h. The findings indicated the leaf and
stem anatomical feature change of wheat plants resulting from adaptation to salinity stress. A reduction
in the anatomical traits of stem and leaf diameter, wall thickness, diameter of the hollow pith cavity,
total number of vascular bundles, number of large and small vascular bundles, bundle length and width,
thickness of phloem tissue, and diameter of the metaxylem vessel of wheat plants was observed. They
also concluded salt stress induces both anatomical and physiological changes in the stem and leaf cells
of wheat, as well as the tissues and organs, and these changes in turn make it possible for the plants to
adapt successfully to a saline environment. They also stated that most plant physiological processes

312
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

associated with salinity are linked to anatomical structure adaptation, which allows plants to grow under
abiotic stress Hameed et al., (2009). For instance, salt stress resulted in physiological and morpho-
anatomic changes in Lotus tenuis Paz et al., (2014). The obtained results on wheat plants grown under
salt stress in terms of the anatomical structures of the main stems and leaves are supported by previous
reports on wheat Akram et al., (2002), kallar grass Abd-Elbar et al., (2012), and faba beans Semida et
al., (2014). Moderate and high salinity concentrations (3000 and 6000 mg.kg−1 NaCl) reduced xylem
and phloem tissue and metaxylem vessel diameter, as well as the primary sorghum bundle size Arafa et
al., (2009). In the present study, seawater salt stress decreased the cross-sectional area of the vascular
bundle throughout the stems and leaflets, resulting in a significantly diminished conductive potential of
the phloem and xylem Fig. (26). Moreover, seawater application reduced the vascular bundle area and
the vessel diameter. Salt stress increased the flowing resistance of water from roots to leaves, reduced
vascular tissue transportation efficiency, and restricted the transportation of water due to dissolved salt
ions absorbed by the roots Akram et al., (2002). However, seawater salt stress had a more visible effect
on phloem than on xylem, in which translocation of water dissolved salt ions was severely restricted to
the ground parts, and the transportation of photosynthetic materials was decreased to the plant apex and
young roots.
Another antioxidant in stress mitigation is glutathione, which can react with superoxide radical,
hydroxyl radical, and hydrogen peroxide, thereby functioning as a free radical scavenger. It can also
participate in the regeneration of ascorbate via ascorbate-glutathione cycle Foyer et al., (1997). When
applied exogenously glutathione helped to maintain plasma membrane permeability and cell viability
during salinity stress in Allium cepa Aly-Salama and Al-Mutawa, (2009). Application of glutathione
and ascorbate was found to be effective in increasing the height of the plant, branch number, fresh and
dry weight of herbs and flowers, and the content of carbohydrates, phenols, xanthophylls pigment, and
mineral ion content when subjected to saline condition Rawia Eid et al., (2011). Many studies have
found differences in levels of expression or activity of antioxidant enzymes; these differences are
sometimes associated with the more tolerant genotype and sometimes with the more sensitive genotype.
Munns and Tester, (2008), suggested that differences in antioxidant activity between genotypes may be
due to genotypic differences in degrees of stomatal closure or in other responses that alter the rate of
CO2 fixation and differences that bring into play the processes that avoid photo inhibition and for which
the plant has abundant capacity Munns and Tester, (2008),. Roy et al., (2014) in their recent review
have argued that there are three main traits in plants, which help them in their adaptation to salinity
stress: ion exclusion, tissue tolerance, and salinity tolerance. It seems that antioxidants have some role
in tissue and salinity tolerance mechanism.

4.5. Roles of Polyamines in Salinity Tolerance.

Polyamines (PA) are small, low molecular weight, ubiquitous, polycationic aliphatic molecules
widely distributed throughout the plant kingdom. Polyamines play a variety of roles in normal growth
and development such as regulation of cell proliferation, somatic embryogenesis, differentiation and
morphogenesis, dormancy breaking of tubers and seed germination, development of flowers and fruit,
and senescence Knott et al., (2007); Galston et al. (1997). It also plays a crucial role in abiotic stress
tolerance including salinity and increases in the level of polyamines are correlated with stress tolerance
in plants Gupta et al., (2013); Kov´acs et al., (2010) Fig. (27).

313
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 27: Illustrates the role of polyamine (PA) in plant abiotic stress tolerance.

The most common polyamines that are found within the plant system are diamine putrescine
(PUT), triamine spermidine (SPD), and tetra-amine spermine (SPM) Alc´azar et al., (2011), Shu et al.,
(2012). The PA biosynthetic pathway has been thoroughly investigated in many organisms including
plants and has been reviewed in details Alet et al., (2012); Rambla et al., (2010) PUT is the smallest
polyamine and is synthesized from either ornithine or arginine by the action of enzyme ornithine
decarboxylase (ODC) and arginine decarboxylase (ADC), respectively Gupta et al., (2013),
Hasanuzzaman et al., (2014). N-carbamoyl-putrescine is converted to PUT by the enzyme N-
carbamoyl-putrescine amino hydrolase Alc´azar et al., (2010); Bouchereau et al., (1999). The PUT thus
formed functions as a primary substrate for higher polyamines such as SPD and SPM biosynthesis. The
triamine SPD and tetramine SPM are synthesized by successive addition of amino propyl group to PUT
and SPD, respectively, by the enzymes spermidine synthase (SPDS) and spermine synthase (SPMS)
Alc´azar et al., (2006); Fluhr and Mattoo, (1996). ODC pathway is the most common pathway for
synthesis of polyamine found in plants. Most of the genes involved in the ODC pathway have been
identified and cloned. However, there are some plants where ODC pathway is absent; for instance in
Arabidopsis polyamines are synthesized via ADC pathway Kusano et al., (2007); Hanfrey et al., (2001).
All the genes involved in polyamine biosynthesis pathways have been identified from different plant
species including Arabidopsis Urano et al., (2003); Janowitz et al., (2003). Polyamine biosynthesis
pathway in Arabidopsis involves six major enzymes: DC encoding genes (ADC1 and ADC2); SPDS
(SPDS1 and SPDS2) and SAMDC (SAMDC1, SAMDC2, SAMDC3, and SAMDC4) Janowitz et al.,
(2003); Hashimoto et al., (1998). On the contrary, single genes represent SPM synthase,
thermospermine synthase, agmatine iminohydrolase and N-carbamoyl putrescine amidohydrolase only
Urano et al., (2004); Hanzawa et al., (2002). Increase in endogenous polyamine level has been reported
when the plant is exposed to salinity stress. Intracellular polyamine level is regulated by polyamine
catabolism. Polyamines are oxidatively catabolized by amine oxidases that include copper binding
diamine oxidases and FAD binding polyamine oxidases. These enzymes play a significant role in stress
tolerance Takahashi and Kakehi, (2010); Cona et al., (2006) Fig. (28).

314
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 28: Metabolism of polyamines in plants. ADC arginine decarboxylase, ODC ornithine
decarboxylase, dcSAM decarboxylated S-adenosylmethionine, SAM S-adenosylmethionine, SAMDC
S-adenosylmethionine decarboxylase, SPDS spermidine synthase, SPMS spermine synthase, PAO
polyamine oxidase, PMT putrescine N-methyltransferase, CuAO copper-dependent amine (diamine)
oxidase. Biosynthesis is indicated by blue arrow and degradation pathway by orange arrow. After
Kamala Gupta et al., (2013)

Kamala Gupta et al., (2013), reported that significance of naturally occurring intracellular
polyamines (PAs), such as spermine, spermidine, and putrescine, in relation to the mechanism and
adaptation to combat abiotic stress has been well established in plants. Because of their polycationic
nature at physiological pH, PAs bind strongly to negative charges in cellular components such as nucleic
acids, proteins, and phospholipids. Accumulation of the three main PAs occurs under many types of
abiotic stress, and modulation of their biosynthetic pathway confers tolerance to drought or salt stress.
Maintaining crop yield under adverse environmental conditions is probably the major challenge faced
by modern agriculture, where PAs can play important role. Over the last two decades, genetic,
transcriptomic, proteomic, metabolomic, and phenomics approaches have unraveled many significant
functions of different PAs in the regulation of plant abiotic stress tolerance. In recent years, much
attention has also been devoted to the involvement of PAs in ameliorating different environmental
stresses such as osmotic stress, drought, heat, chilling, high light intensity, heavy metals, mineral
nutrient deficiency, pH variation, and UV irradiation
The changes in cellular polyamine level due to stress provide possible implications in stress but
do not provide evidence of their role in counteracting stress. Hence, to understand whether polyamines
actually protect cells from stress-induced damages, exogenous application of polyamines, which is
expected to increase endogenous polyamine, has been investigated before or during stress Tisi et al.,
(2008); Navakoudis et al., (2003). Application of exogenous polyamine has been found to increases the
level of endogenous polyamine during stress. Positive effects of polyamines have been associated with
the maintenance of membrane integrity, regulation of gene expression for the synthesis of osmotically
active solutes, reduction in ROS production, and controlling accumulation of Na+ and Cl− ion in
different organs Tisi et al., (2008); Yiu, et al., (2009). It was observed that plant deficient in ADC1 and
ADC2 is hypersensitive to stress Hussain et al., (2011). In Arabidopsis, expression of ADC and SPMS
increases when exposed to salinity stress. Whereas mutants of polyamine biosynthetic genes show
sensitivity to salinity Yamaguchi et al., (2006). Overproduction of PUT, SPD, and SPM in rice, tobacco,
and Arabidopsis enhances salt tolerance Roy and Wu, (2002). Salt stress regulates polyamine
biosynthesis and catabolism by acting as a cellular signal in hormonal pathways thereby regulating
abscisic acid (ABA) in response to stress Shevyakova et al., (2013). Additionally, SPM and SPD are
regarded as potent inducers of NO that is another important signalling molecule Moschou et al., (2008)
and its involvement in salinity tolerance is discussed below. It has been reported that exogenous
application of polyamines could alleviate salt-induced reduction in photosynthetic efficiency, but this
effect depends on polyamine concentration, types, and level of stress Duan et al., (2008). When the

315
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

seedling of Sorghum bicolor treated with 0.25mM SPM is subjected to salt stress it shows improvement
in growth and partial increase in the activity of peroxidase and glutathione reductase enzyme with a
concomitant decrease in the level of membrane lipid peroxidation Chai et al., (2010); Li et al., (2013)
performed 2-DE gel electrophoresis and MALDITOF/ TOFMS with cytosolic proteins to understand
the effect of exogenous SPD on proteomic changes under normal and NaCl stress of 3 days old
cucumber seedling leaves. Many changes were observed in the levels of proteins involved in energy
and metabolic pathways, protein metabolic, stress defense, and other functional proteins. They observed
that increased salt tolerance by exogenous SPD would contribute to higher expressions of proteins
involved in the SAMs metabolism, protein biosynthesis, and defense mechanisms on antioxidant and
detoxification. Li et al., (2013) also argued that the regulation of Calvin cycle, protein-folding assembly,
and the inhibition of protein proteolysis by SPD might play important roles in salt tolerance.

4.6. Roles of Nitric Oxide in Salinity Tolerance.

Nitric oxide (NO) is a small volatile gaseous molecule, which is involved in the regulation of
various plant growth and developmental processes, such as root growth, respiration, stomata closure,
flowering, cell death, seed germination and stress responses, as well as a stress-signalling molecule
Delledonne et al. (1998), Crawford (2006). NO directly or indirectly triggers expression of many redox-
regulated genes. NO reacts with lipid radicals thus preventing lipid oxidation, exerting a protective
effect by scavenging superoxide radical and formation of peroxynitrite that can be neutralized by other
cellular processes. It also helps in the activation of antioxidant enzymes (SOD, CAT, GPX, APX, and
GR) Bajgu (2014) Fig. (29).

Fig. 29: Potential mechanisms of NaCl stress mitigation by application of exogenous NO. Excessive
NaCl causes osmotic and oxidative stresses in plants. Salt stress induces ABA accumulation, which
promotes H2O2 generation through NAD (P) H oxidase. Stress-induced H2O2 triggers generation of
endogenous NO by activating NR (nitrate reductase) and NOS (nitric oxide synthase)-like enzymes.
Exogenous application of NO to plants may enhance the biosynthesis of endogenous NO, as well as
that of antioxidant enzymes through MAPK (mitogen-activated protein kinase) and other unknown
signaling pathways. Exogenous NO supplementation to plants can also up-regulate genes involved in
proline synthesis, such as P5CS1, and other stress-related genes responsible for NaCl tolerance, whereas
it might down-regulate ProDH that is involved in proline catabolism. Exogenous NO treatment may
also help balance osmotic homeostasis in plants under salt stress via the SOS (salt overly sensitive)
pathway, by increasing plasma membrane H+-ATPase activity. APX, ascorbate peroxidase; AsA,
ascorbic acid; CAT, catalase; GR, glutathione reductase; H2O2, hydrogen peroxide; P5CS1, δ1-
pyrroline-5-carboxylate synthetase; ProDH, proline dehydrogenase; ROS, reactive oxygen species;
SOD, superoxide dismutase; TFs, transcription factors. After Ahmad et al. (2016)

Ahmad et al. (2016) reprted that External application of nitric oxide (NO) in the form of its donor
S-nitroso-N-acetylpenicillamine (SNAP) could mitigate the deleterious effects of NaCl stress on
chickpea (Cicer arietinum L.) plants. SNAP (50 µM) was applied to chickpea plants grown under non-

316
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

saline and saline conditions (50 and 100 mM NaCl). Salt stress inhibited growth and biomass yield, leaf
relative water content (LRWC) and chlorophyll content of chickpea plants. High salinity increased
electrolyte leakage, carotenoid content and the levels of osmolytes (proline, glycine betaine, soluble
proteins and soluble sugars), hydrogen peroxide (H2O2) and malondialdehyde (MDA), as well as the
activities of antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT), ascorbate
peroxidase (APX), and glutathione reductase in chickpea plants. Expression of the representative SOD,
CAT and APX genes examined was also up regulated in chickpea plants by salt stress. On the other
hand, exogenous application of NO to salinized plants enhanced the growth parameters, LRWC,
photosynthetic pigment production and levels of osmolytes, as well as the activities of examined
antioxidant enzymes that is correlated with up-regulation of the examined SOD, CAT and APX genes,
in comparison with plants treated with NaCl only. Furthermore, electrolyte leakage, H2O2 and MDA
contents showed decline in salt-stressed plants supplemented with NO as compared with those in NaCl-
treated plants alone. Thus, the exogenous application of NO protected chickpea plants against salt
stress-induced oxidative damage by enhancing the biosynthesis of antioxidant enzymes, thereby
improving plant growth under saline stress. Taken together, our results demonstrate that NO has
capability to mitigate the adverse effects of high salinity on chickpea plants by improving LRWC,
photosynthetic pigment biosynthesis, osmolyte accumulation and antioxidative defense system.
Exogenous NO application has been found to play roles in stress mitigation Sung and Hong
(2010), Xiong et al. (2010), but the effects depend on NO concentration Fig. (30).

Fig. 30: Sources of NO production and NO functions in regulating plant growth, development, and
adaptive processes. The reductive pathway is based on the reduction of nitrite to NO, whereas the
oxidative route relies on the oxidation of aminated molecules, such as L-Arg. The produced NO can be
used to transduce external and internal signals to regulate plant development and stress responses by
interacting with other cellular messengers. NR, nitrate reductase; Ni: NOR, NO-forming nitrite
reductase; mETC, mitochondrial nitrite reduction; NOS, nitric oxide synthase; L-Arg, L-arginine; PA,
polyamine; HA, hydroxylamine. After Sun et al. (2021)

Sun et al. (2021) stated that nitric oxide (NO) regulates plant growth, enhances nutrient uptake,
and activates disease and stress tolerance mechanisms in most plants, making NO a potential tool for
use in improving the yield and quality of horticultural crop species. Although the use of NO in
horticulture is still in its infancy, research on NO in model plant species has provided an abundance of
valuable information on horticultural crop species. Emerging evidence implies that the bioactivity of
NO can occur through many potential mechanisms but occurs mainly through S-nitrosation, the
covalent and reversible attachment of NO to cysteine thiol. In this context, NO signaling specifically
affects crop development, immunity, and environmental interactions. Moreover, NO can act as a
fumigant against a wide range of postharvest diseases and pests. However, for effective use of NO in
horticulture, both understanding and exploring the biological significance and potential mechanisms of

317
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

NO in horticultural crop species are critical. This review provides a picture of our current understanding
of how NO is synthesized and transduced in plants, and particular attention is given to the significance
of NO in breaking seed dormancy, balancing root growth and development, enhancing nutrient
acquisition, mediating stress responses, and guaranteeing food safety for horticultural production
Exogenous application of sodium nitroprusside (SNP), a NO donor, on Lupinus luteus seedlings
subjected to salt stress enhanced seed germination and root growth Kopyra and Gw´o´zd´z (2003) .Seed
germination was promoted at concentrations between 0.1 and 800 M SNP in a dose-dependent manner.
Stimulation was most pronounced effects after 18 and 24 h and ceased after 48 h of imbibition. The
promoting effect of NO on seed germination persisted even in the presence of heavy metals (Pb and
Cd) and NaCl. Kopyra and Gw´o´zd´z (2003) further showed that the pretreatment of L. luteus seedlings
for 24 h with 10 M SNP resulted in efficient reduction of the detrimental effect of the abiotic stressors
on root growth and morphology. Pretreatment of maize seedlings with 100 MSNP increases dry matter
of roots and shoots under salinity stress; however, when the concentration of SNP was increased to
1000 M shoot and root dry weight decreased Zhang et al. (2006). Thus, this experiment highlighted
both the protective effects of low NO concentration and the toxic effect of high NO concentration on
plants. The positive effects of NO on salinity tolerance attributed to antioxidant activities and
modulation of ROS detoxification system Mishra et al. (2011). Improved plant growth under salinity
stress by exogenous application of NO was associated with increases in antioxidant enzymes such as
SOD, CAT, GPX, APX, and GR Zhao et al. (2004), and suppression of malondialdehyde (MDA)
production or lipid peroxidation Nalousi et al. (2012). Effects of NO on salinity tolerance are related to
its regulation of plasma membrane H+-ATPase and Na+/K+ ratio Crawford (2006). NO stimulates H+-
ATPase (H+-PPase), thereby producing a H+ gradient and offering the force for Na+/H+ exchange. Such
an increase of Na+/H+ exchange may contribute to K+ and Na+ homeostasis Zhang et al. (2006).
Although NO acts as a signal molecule under salt stress and induces salt resistance by increasing PM
H+-ATPase activity, research results from Zhang et al. (2007) with calluses from Populus euphratica
also indicated NO cannot activate purified PM H+-ATPase activity, at least in vitro. They initially
hypothesized ABA or H2O2 might be downstream signal molecules to regulate the activity of PM H+-
ATPase. Further results indicated H2O2 content increased greatly under salt stress. Since H2O2 might be
the candidate downstream, signal molecule, Zhang et al. (2007) tested PM H+-ATPase activity and K
to Na ratio in calluses by adding H2O2. The results suggested that H2O2 inducing an increased PM H+-
ATPase activity resulted in an increased K to Na ratio leading to NaCl stress adaptation.

4.7. Hormone Regulation of Salinity Tolerance.

Abscisic acid (ABA) is important phytohormones whose application to plant ameliorates the
effect of stress condition(s). Salinity stress causes osmotic stress and water deficit, increasing the
production of ABA in shoots and roots He and. Cramer (1996), Popova et al. (1995). Accumulation of
ABA can mitigate the inhibitory effect of salinity on photosynthesis, growth, and translocation of
assimilates Popova et al. (1995), Jeschke et al. (1997) Fig. (31). The positive relationship between ABA
accumulation and salinity tolerance has been at least partially attributed to the accumulation of K+, Ca2+
and compatible solutes, such as proline and sugars, in vacuoles of roots, which counteract with the
uptake of Na+ and Cl− Chen et al. (2001), Gurmani et al. (2011).

318
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 31: Illustrates salt stress stimulated the accumulation of endogenous ABA in the root tips and LRs.
(A) Observations of the distribution of ABA accumulation by immunofluorescence in PRs subjected to
0, 100, and 200 mM NaCl via confocal microscopy. Bars = 100 µm. (B) Observations of ABA
localization by immunofluorescence in transverse root sections in the presence of 0, 100, and 200 mM
NaCl under confocal microscopy. The curve on the right of the picture shows the ABA/Alexa Fluor 555
fluorescence intensity. En, endodermis; Pc, pericycle; Ph, Phloem. Bars = 50 µm. (C) Fluorescence
intensity (%) of fluorescence portion in picture (A). The data represent the means ± SEs of five
replicates, with 10 seedlings each. N, NaCl. (D) Fluorescence intensity (%) of the fluorescence part in
picture (B). The data represent the means ± SEs of five replicates, with 10 seedlings each. N, NaCl. (E)
Observations via confocal microscopy of the ABA distribution and concentration at different
developmental stages of LRs subjected to 0 mM or 200 mM NaCl treatment for 8 h. Bars = 50 µm. The
figures were selected from five replicates, with 10 seedlings per replicate. The different letters represent
significant differences (P < 0.05, based on Student's t-test). After Lu et al. (2019)

Lu et al. (2019) reported that root architectures are important organs in plant. Lateral root (LR)
initiation (LRI) and development play a central role in environmental adaptation. The mechanism of
LR development has been well investigated in Arabidopsis. When we evaluated the distribution of auxin
and abscisic acid (ABA) in maize, we found that the mechanism differed from that in Arabidopsis. The
distribution of ABA and auxin within the primary roots (PRs) and LRs was independent of each other.
Auxin localization was observed below the quiescent center of the root tips, while ABA localized at the
top of the quiescent center. Furthermore, NaCl inhibited LRI by increasing ABA accumulation, which
mainly regulates auxin distribution, while auxin biosynthesis was inhibited by ABA in Arabidopsis.
NaCl and exogenous ABA disrupted the polar localization of ZmPIN1 in maize. An inhibitor of ABA
biosynthesis, fluridone (FLU), and the ABA biosynthesis mutant vp14 rescued the phenotype under
NaCl treatment. Together, all the evidence suggested that NaCl promoted ABA accumulation in LRs
and that ABA altered the polar localization of ZmPIN1, disrupted the distribution of auxin and inhibited
LRI and development Fig. (31).
ABA is a vital cellular signal that modulates the expression of a number of salt and water deficit-
responsive genes. Fukuda and Tanaka (2006) demonstrated the effects of ABA on the expression of
two genes, HVP1 and HVP10, for vacuolar H+-inorganic pyrophosphatase, and of HvVHA-A, for the
catalytic subunit (subunit A) of vacuolar H+-ATPase in Hordeum vulgare under salinity stress. ABA
treatment in wheat induced the expression of MAPK4-like, TIP 1, and GLP 1 genes under salinity stress

319
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Keskin et al. (2010). Some other compounds having hormonal properties, such as salicylic acid (SA)
and brassinosteroids (BR), also participate in plant abiotic stress responses Fragnire et al. (2011), Clause
and Sasse (1998). Under salinity stress, endogenous level of SA increased along with the increase in
the activity of salicylic acid biosynthetic enzyme in rice seedling Sawada et al. (2006). Jayakannan et
al. (2013) have recently shown that SA improves salinity tolerance in Arabidopsis by restoring
membrane potential and preventing salt-induced K+ loss via a guard cell outward rectifying K+ (GORK)
channel. Arabidopsis seedling pretreated with SA showed upregulation of H+-ATPase activity, thereby
improving K+ retention during salt stress; SA pretreatment did not prevent accumulation of Na+ in roots
but somehow helped to reduce the concentration of accumulated Na+ in the shoot Jayakannan, et al.
(2013) .The application of SA also promoted salinity tolerance in barley, as manifested by increases in
the content of chlorophyll and carotenoid and maintaining membrane integrity, which was associated
with more K+ and soluble sugar accumulation in the root under saline condition El-Tayeb (2005), Nazar,
et al. (2011) have argued that SA alleviates decreases in photosynthesis under salt stress by enhancing
nitrogen and sulfur assimilation and antioxidant metabolism differentially in mung bean cultivars. BR
El-Mashad and. Mohamed (2012), Ashraf et al. (2010) may also mitigate the negative effects of salinity.
Application of BR enhanced the activity of antioxidant enzymes (SOD, POX, APX, and GPX) and the
accumulation of nonenzymatic antioxidant compounds (tocopherol, ascorbate, and reduced glutathione)
El-Mashad and. Mohamed (2012). Both BRs and SA are ubiquitous in the plant kingdom, affecting
plant growth and development in many different ways, and are known to improve plant stress tolerance.
Ashraf, et al., (2010), have reviewed and discussed the current knowledge and possible applications of
BRs and SA that could be used to mitigate the harmful effects of salt stress in plants. They have also
discussed the roles of exogenous applications of BRs and SA in the regulation of various biochemical
and physiological processes leading to improved salt tolerance in plants.

5. Role of Silicon in Salinity Tolerance

5.1. Mechanisms of Silicon in Alleviating Salinity Stress
Salinity stress is one of the most common environmental stresses that pose threats to the
agriculture industry worldwide. The effects of salinity stress on plants are mainly manifested in the
following areas. (a) Osmotic stress caused by excessive soluble salt in the soil decreases the osmotic
potential of soil solutions and decreases the ability of plant root systems to absorb water, resulting in
physiological drought. (b) Ion toxicity results from the toxic effect of salt ions like Na+ and Cl- inside
plant cells. Excessive accumulation of intracellular salt ions results in ion imbalance and metabolic
disorders. (c) Secondary stresses causing by osmotic and ionic stresses, including the accumulation of
toxic compounds like ROS and disruption of nutrient balances in plants. For example, under high
salinity conditions, Na+ competes with Ca2+ and K+ in the cell membrane, resulting in reproductive
disorders Zhu (2016). In recent years, there have been a large number of reports about the roles of Si in
alleviating salinity-induced ion stress and oxidative damage Wu et al. (2015), Debona et al., (2017),
Luyckx et al., (2017) Fig. (32).

320
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 32: Presents a schematic model for the beneficial impact of silicon on plant under salt stress. Six
main strategies are involved in Si's alleviation of salt stress: For strategy I, Si could enhance
photosynthesis by maintaining the integrity of photosynthetic organs, increasing the CO2 utilization rate
in plants and increasing the openness and activity of the PSII reaction center. For strategy II, Si regulates
ion homeostasis through mediating Na + uptake, transport, and compartmentalization, and
corresponding gene expression (e.g., NHX and HKT). For strategy III, Si can regulate the
activity/concentration of enzymatic and/or nonenzymatic antioxidants and endogenous polyamine
accumulation to alleviate oxidative damage caused by salinity stress. For strategy IV and V, Si enhances
the root hydraulic conductance through regulating aquaporin activities and improving osmoregulatory
capacities, which contributes to an increase in water uptake and transport. For strategy VI, Si may
mediate ion homeostasis and decrease oxidative damage through regulating polyamine metabolism.
Single solid black line ended with bar: process of mediating. Single dash black line: speculated
mechanisms that need to be experimentally proved. Red arrow: increase (up) or decrease (down). '?'
represents mechanisms that are different between species. Chloroplast and mitochondrion component
in this schematic model are modified from Yamori (2016). After Zhu et al (2019)

Recently, progresses have been made in elucidating the alleviative effects of Si in salt-induced
osmotic stress Zhu et al., (2015), oxidative damage Yin et al., (2019), and Na+ accumulation Flam-
Shepherd et al., (2018). Thus, this review covered the latest research. In addition, because of the
available published results, a model describing how Si is involved in alleviating salt stress damage was
proposed. We also proposed further studies that are required to address these mechanisms.

5.2. Modulation of Seed Germination, Plant Growth, and Photosynthesis

5.2.1. Seed Germination
Seed is a crucial organ in higher plants. Seed germination and early seedling growth signify a
key stage in the plant life cycle Karunakaran, etal. (2013). Si significantly increases germination
characteristics (e.g., germination percentage, germination rate and shoot length) under both normal and
stress (e.g., salt/drought) conditions Shi, etal. (2014), Karunakaran, etal. (2013). The mechanisms for
Si-mediated salt tolerance in seed germination stage still remain obscure, but have been proposed to be
associated with the alleviated oxidative stress Shi, etal. (2014), Karunakaran, etal. (2013). In mung bean
under salt stress, application of Si and salicylic acid (SA) was reported to improve seed physiological
quality through increasing K+ and decreasing Na+ accumulation in seeds Lotfi, etal. (2015). Till now,
the interaction between Si and hormones (e.g., abscisic acid and gibberellins), which play a role in

321
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

controlling seed development and germination, are still not fully understood Sah, etal. (2016). Thus, to
further reveal the mechanisms of Si-mediated salt tolerance during seed germination, studies are needed
to elucidate changes in hormones and hormone-responsive genes in response to salt stress and Si
treatment. The use of Si-uptake mutants can aid researchers to better understand the biochemical
function of Si in plant growth and development, in which physical barrier induced by Si deposition on
seed surface could be partly excluded. Under salinity stress, Zhang, et al. (2009) studied the effects of
Si on the germination of Si-mutant rice seeds that accumulate less Si in the shoot Ma (2002). Their
results showed that the application of exogenous Si increased the bud length, bud weight, and
germination rate more obvious in mutant rice than the wild type rice. This might be due to the changes
in the mutant seed embryo and seed coat, which enables it to utilize Si more efficiently. The study of
Isa, etal. (2002) found that even though the Si-mutant rice forms relatively less SiO2 bodies in the leaves,
Si application could still significantly promote the growth of these mutants, suggesting that Si
participates in the physiological and biochemical processes of rice. Actually, Laane (2017), (2018)
proposed that foliar SA and nano-SiO2 could be classified as biostimulants (‘plant growth promoter’)
that enhance nutritional efficacy and decrease abiotic and biotic stresses. The Si-uptake mutants should
be investigated further to better understand the alleviating mechanisms of Si, including its potential
biostimulants functions, in seed germination under salinity stress.

5.2.2. Plant Growth and Photosynthesis

The enhancement of plant shoot and/or root growth by Si under salt stress have been reported in
many plant species, such as rice, maize, wheat, cucumber, tomato, and so on Wu etal (2015) Fig.
(33),(34).

Fig. 33: Experimental setup of mung bean (Vigna radiata) under 1mM (Si1) and 5mM (Si2) Si supply
and salinity stress after eight treatments: (i) control (T1), (ii) −NaCl+Si (1mM/5mM) (T2), (iii) 10mM
NaCl/−Si (T3), (iv) 10mM NaCl/+Si (1mM/5mM) (T4), (v) 20mM NaCl/−Si (T5), (vi) 20mM NaCl/+Si
(1mM/5mM) (T6), (vii) 50mM NaCl/−Si (T7), and (viii) 50mM NaCl/+Si (1mM/5mM) (T8) for a
period of 10days. After Musa Al Murad and Sowbiya Muneer, (2021).

Roots play a key role in plant development and are the first tissue to perceive salt stress. Si has
been reported to regulate root growth and architecture of salt-stressed plants Zhu, etal. (2015), Kim,
etal. (2014), in cucumber, Si was found to increase the root–shoot ratio of salt-stressed plants and
improve root hydraulic conductance, likely accounting for improved plant water balance Wang, etal.
(2015) Fig. (34).

322
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 34: Changes in the formation of root nodules of mung bean (Vigna radiata) under (A) 1mM (Si1)
and (B) 5mM (Si2) Si supply and salinity stress after eight treatments: (i) control (T1), (ii) −NaCl+Si
(1mM/5mM) (T2), (iii) 10mM NaCl/−Si (T3), (iv) 10mM NaCl/+ Si (1mM/5mM) (T4), (v) 20mM
NaCl/−Si (T5), (vi) 20mM NaCl/+Si (1mM/5mM) (T6), (vii) 50mM NaCl/−Si (T7), and (viii) 50mM
NaCl/+Si (1mM/5mM) (T8) for a period of 5 and 10days. Vertical bars indicate Mean±SE of the means
for n=4. Means denoted by the different letters are significantly different at p≤0.05 according to the
Tukey’s studentized range test. Musa Al Murad and Sowbiya Muneer, (2021).

In rice and sorghum, Si might improve root growth by promoting Casparian band formation and
stimulating suberin and lignin biosynthesis or by increasing cell wall extensibility in the growth region
Hattori, etal. (2003) Fleck, etal. (2015). Plant growth and yield depend largely on photosynthesis
Chaves, etal. (2008). the salinity stress-induced growth inhibition in plants can be attributed to stress-
induced reduction in photosynthesis. From the large amount of data available on the improvement effect
of Si on shoot growth and net photosynthetic rate, it is reasonable to speculate that Si might function to
maintain a high photosynthetic rate in salt-stressed plants Zargar, etal. (2019), Coskun, etal. (2019),
Yin, etal. (2013). the reason why salinity stress results in reduced photosynthetic rate in plants includes
the following aspects. (a) Modification of the structure and function of organelles that are responsible
for photosynthesis; (b) ion toxicity and oxidative stress to thylakoid membranes and other cellular
components; (c) osmotic stress-induced reduction in CO2 assimilation rate, which enhances stomatal
closure and CO2 availability; and (d) inhibition of the transfer of assimilation products Chaves, etal.
(2008), Yamori (2016). Accordingly, the mechanisms by which Si improves plant photosynthesis under
salinity stress can be summarized as follows. (A) The addition of Si under salinity stress can decrease
ion toxicity and ROS accumulation to maintain the structure and function of organelles that are
responsible for photosynthesis Liang (1999), Liang, etal. (2003), (B) The decreased photosynthetic rate
is also due to the reduction in stomatal conductance and nonstomatal inhibition, resulting in restricted
availability of CO2 for carboxylation reactions. Abbas, et al. (2015) found that Si supplementation in
two okra (Abelmoschus esculentus) cultivars with different salt tolerance could increase stomatal
conductance, transpiration rate, and number and size of stomata, leading to efficient photosynthetic
activity under salinity stress. These results showed that Si supplication under salinity stress could
improve photosynthesis by maintaining the integrity of photosynthetic organs and photosynthetic
pigment levels and by increasing the CO2 utilization rate in plants Fig. (35)

323
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 35: Illustrates nanoparticle-induced regulation of carbohydrate metabolism, photosynthesis, and

ROS homeostasis in solanum lycopersicum Subjected to Salinity Stress, Alam et al., (2022)

(D) Salinity stress affects the transport and allocation of photosynthetic products. This results in
the accumulation of photosynthetic products such as sucrose and starch, causing feedback inhibition of
photosynthesis and decreasing plant growth. Currently, relatively few systematic studies have been
conducted on the effects of Si on carbohydrate metabolism. In cucumber, Zhu, et al., (2016)
demonstrated that Si application decreased the soluble sugar and starch content in leaves, but increased
the starch content in roots through mediating the activities of carbohydrate metabolism enzymes, and
thus alleviated photosynthetic feedback repression in leaves and provided more energy storage for root
growth. However, experimental evidence is still lacking in this study. Thus, molecular biology
approaches should be used to further reveal the mechanisms by which Si affects carbohydrate
metabolism, antioxidants system, polyamine accumulation, and water relationship. However, whether
Si regulates these metabolisms directly. In recent years, chlorophyll fluorescence parameters have been
widely used to study various photosynthetic reactions under stress conditions Gorbe, (2012).
Photosystem II (PS II) appears to be a salt stress-sensitive component of the photosynthetic system
Parihar et al., (2015). In cucumber, salinity stress significantly decreased the Fv’/Fm’ (PSII effective
photochemical efficiency), Fv/Fm (PSII maximum photochemical efficiency), qP (photochemical
quenching coefficient), and FPSII (PSII actual photochemical efficiency), whereas it significantly
increased the NPQ (non-photochemical quenching coefficient). However, Si application could increase
Fv/Fm, Fv’/Fm’, FPSII, and qP, and decrease NPQ during salinity stress Zhu et al., (2015). Similarly,
in salt-stressed aloe, Si application was reported to decrease minimum fluorescence (FO), and increase
variable fluorescence (Fv) and the potential activity of photosystem II (PSII), thus improving
photosynthetic efficiency in aloe Munns and Tester, (2008). These results showed that the addition of
Si helps to increase the openness and activity of the PSII reaction center, facilitating the use of more
energy in PSII electron transfer and increasing the efficiency of converting light energy into chemical
energy Zhu et al., (2015). In conclusion, Si enhances photosynthesis in salt-stressed plants by
decreasing salt-ion accumulation, scavenging ROS, and regulating carbohydrate metabolism. However,
further in-depth research is needed to understand the molecular mechanisms of how Si regulates ROS
and carbohydrate metabolism, such as its regulatory effects on the gene expression levels of related
enzymes.

5.2.3. Silicon and Ion Homeostasis Regulation

High concentrations of salt ions, particularly Na+ and Cl- ions generally affect the absorption of
other nutrients (such as potassium and calcium) by plants and cause increased cell membrane
permeability, resulting in metabolism disorders and dysregulation Xu et al., (2015). To cope with salt
stress, the plant can reduce Na+ uptake, increase Na+ efflux, and compartmentalization of Na+ in the
vacuole to reduce cytoplasmic ion toxicity Parida and Das, (2005) Fig. (36).

324
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 36: Intracellular Na+ homeostasis mediated by Na+ transporters, channels, and their regulatory
elements. In this figure, 1 stands for plasma membrane (PM) H+-ATPase, 2 stands for tonoplast (TP)
H+-ATPase and 3 stands for TP H+-pyrophosphatase. Some new components in these transport
mechanisms have recently been added, i.e., the regulation of stelar-localized SOS1 activity by Nax1
and Nax2 Na+ exclusion loci in rice. This regulation improves salt stress tolerance by enhancing the
retrieval of Na+ from xylem back into stellar cells. Another component is the potential involvement of
plant aquaporins (AQP, AtPIP2;1 in particular) in Na+ uptake. Equally important is the role of FV (fast
vacuolar) and SV (slow vacuolar) channels that mediate vacuolar Na+ leakage to the cytosol, deemed a
salt-sensitive trait. Worthy of note also is the role of PM and TP H+ pumps that generate a pmf to
energize Na+ transport via the two Na+/H+ exchangers (SOS1 and NHXs), as well as the importance of
Na+ efflux from chloroplasts mediated by the chloroplastic sodium hydrogen antiporter (NHD1). The
NADPH dehydrogenase (NDH)-dependent cyclic electron flow (CEF) constitutes an important source
of ATP required to fuel Na+ sequestration into vacuoles. Red line indicates inhibition, while black
arrows indicate activation. After Assaha et al., (2017)

Accordingly, the possible mechanisms by which Si regulates ion homeostasis under salt stress
can be classified into three main categories as follows.

5.2.4. Silicon Restricts Na+ Uptake and Transport

Studies on the mechanisms by which Si alleviates salinity stress in plants are mostly focused on
decreasing Na+ in the root and/or shoot. For example, the addition of Si to salt-stressed barley could
significantly decrease the levels of Na+ and Cl- in the root system, with Na+ and K+ being more evenly
distributed throughout the entire root. This has been regarded as one of the major mechanisms by which
Si alleviates salinity stress in barley Liang, (1999). In salt-stressed alfalfa (Medicago sativa L.), Si
application significantly decreases Na+ levels in the roots, but has no effects on Na+ accumulation
unclear whether Na+ decrease along with Si addition is due to the changes in the root structure and/or a
reduction in the transpiration stream in the xylem, which need to be studied in more species, in the shoot
Wang et al., (2007). In wheat, Tuna et al., (2008) reported that the addition of Si could simultaneously
decrease Na+ accumulation in both shoot and root. Garg and Bhandari, (2016) found that the addition
of Si decreases Na+ absorption in the root system and translocation toward the leaves, as well as
increases the K+/Na+ ratio, in chickpeas (Cicer arietinum L.). However, the mechanisms for these
reductions are still largely unknown in most species except in rice. In rice, Si application showed an
increased formation of Casparian bands in the exodermis and endodermis Fleck et al., (2015), Fleck
and Nye, (2011) which might partly hinder the penetration of Na+ ions into the symplast and/or
transpiration stream Wu et al., (2015); Guerriero et al., (2016). Accordingly, Gong et al., (2006) showed
that in rice (‘IR36’), the addition of Si did not change Na+ levels in the root but decreased the upward
transport of Na+ through apoplastic pathway Fig. (37).

325
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Pannaga Krishnamurthy et al., (2009) reported that increasing soil salinity reduces crop yields
worldwide, with rice being particularly aVected. We have examined the correlation between apoplastic
barrier formation in roots, Na+ uptake into shoots and plant survival for three rice (Oryza sativa L.)
cultivars of varying salt sensitivity: the salt-tolerant Pokkali, moderately tolerant Jaya and sensitive
IR20. Rice plants grown hydroponically or in soil for 1 month were subjected to both severe and
moderate salinity stress. Apoplastic barriers in roots were visualized using Xuorescence microscopy
and their chemical composition determined by gas chromatography and mass spectrometry. Na+ content
was estimated by Xame photometry. Suberization of apoplastic barriers in roots of Pokkali was the most
extensive of the three cultivars, while Na+ accumulation in the shoots was the least. Saline stress induced
the strengthening of these barriers in both sensitive and tolerant cultivars, with increase in mRNAs
encoding suberin biosynthetic enzymes being detectable within 30 min of stress. Enhanced barriers
were detected after several days of moderate stress. Overall, more extensive apoplastic barriers in roots
correlated with reduced Na+ uptake and enhanced survival when challenged with high salinity.

Fig. 37: Development of aerenchyma and Casparian bands in rice roots. a Aerenchyma development
(1–6). Cross-sections were made from 1-month-old rice roots grown in hydroponic culture. Images of
sections made at 30 mm (1, 4), 50 mm (2, 5) and 100 mm (3, 6) from the root tip in Pokkali and IR20
under control conditions. b Casparian bands in the endodermis (1–8). Freehand cross-sections were
stained with berberine-aniline blue and viewed using blue light. Arrowheads show Casparian bands in
the endodermis. Control (1, 5) and stressed Pokkali (2, 6) at 20 mm and 30 mm. Control (3, 7) and
stressed IR20 (4, 8) at 20 mm and 30 mm. c Casparian bands in the exodermis (1–12) stained with
berberine-aniline blue. Freehand cross-sections taken at 10 mm (1, 2), 20 mm (5, 6) and 30 mm (9, 10)
of control and stressed Pokkali, respectively. Sections at 10 mm (3, 4), 20 mm (7, 8), and 30 mm (11,
12) from root tip of control and stressed IR20, respectively. Arrowheads show Casparian bands in the
exodermis. Numbers indicate the distance from the root tip. ae aerenchyma, co cortical cells, rh
rhizodermis. Bars 100 µm (b), 50 µm (c). After Pannaga Krishnamurthy et al., (2009)

However, most recently, Flam-Shepherd et al., (2018) measured the radiotracer fluxes of 24 Na+
and proposed that Si does not affect Na+ transport across cell membranes and within the bulk root
apoplast. Moreover, their study revealed that Si reduced Na+ translocation via bypass flow only in the
salt-tolerant (‘Pokkali’) rice cultivars, but not in the salt-sensitive (‘IR29’) ones, in which the bypass
flow was small and not affected by Si. The decline in the shoot Na+ concentration of salt-sensitive
(‘IR29’) rice cultivars can be explained by the pronounced stimulation of leaf growth and shoot-to-root
ratio. Therefore, much more remains to be explored about the effect of Si on Na+ dynamics across

326
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

membranes and through extracellular space in plants. However, many determinants have not been
studied in sufficient detail in salt-stressed plants with or without silicon addition, such as the Na+ signal
perception process. Moreover, it is unclear whether Na+ decrease along with Si addition is due to the
changes in the root structure and/or a reduction in the transpiration stream in the xylem.

5.2.5. The Regulatory Mechanisms Mediating Na+ Compartmentalization

Excessive Na exclusion, or its compartmentation into vacuoles, is an important adaptive strategy
for plants in response to salt stress Farooq et al., (2015). Na+/H+ antiporter protein plays an extremely
important role in Na+ flux and vacuole partitioning Zhao et al., (2017). In higher plants, the H+-ATPases
located on the cell membrane utilize the energy generated from ATP hydrolysis to pump H+ out of the
cells to generate a transmembrane proton gradient. This provides a driving force for the Na+/H+
antiporter protein on the plasma membrane. The Na+ is expelled out of the cells against an
electrochemical gradient when H+ is transported into the cells along an electrochemical gradient
Blumwald, (2000); Liang et al., (2005). Previous studies showed that compared to the salinity stress
alone, Si application significantly increased the activities of H+-ATPases on the plasma membrane, as
well as the activities of H+-ATPase and H+-PPase on vacuolar membranes in the roots of barely Liang,
et al. (2005). The Si-mediated elevation of the H+-ATPase activity was conducive for the expulsion of
Na+ out of the cell, while the elevation in the activities of H+-ATPase and H+-PPase in vacuolar
membranes facilitates the distribution of Na+ into vacuoles, thereby decreasing the Na+ toxicity in the
root Liang et al. (2005), (2006). However, further studies are required to determine whether Si can
directly regulate the activity of the Na+/H+ antiporter and H+-ATPase on the plasma membrane and
vacuolar membranes. Fig. (38), (39).

Fig. 38: Presents the Si transport in a typical grass species. Silicic acid from the soil is transported into
the root symplast by the action of aquaporins such as Lsi1 channels. The silicic acid then diffuses across
the root into the endodermis. At the endodermis, Lsi2 transports silicic acid into the stelar apoplast from
where it diffuses into the xylem and is transported to the shoot in the transpiration stream. In rice, the
presence of aerenchyma means that Lsi2 is localized at both the exodermis and endodermis. In the
shoot, silicic acid is unloaded from the xylem by further aquaporins such as Lsi6 and deposited in the
cell walls and in specific silica cells. Based on Ma and Yamaji, (2015). After Thorne et al., (2020)

327
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 39: Illustrates the effect of Si on oxidative stress. (1) Under abiotic stress conditions, accumulation
of reactive oxygen species (ROS) inside the cell causes protein oxidation, lipid oxidation (resulting in
increased electrolyte leakage out of the cell), and activation of stress response genes. (2) During drought
stress, Si increases the root hydraulic conductance and stomatal conductance, but reduces cuticular
transpiration (5). On balance, this can allow more water to enter the cell and thus reduce the
accumulation of ROS. (3) During salt stress, as well as improving the plant water status, Si reduces Na+
and Cl- accumulation in shoot by forming endodermal barriers in the root. This reduces the
accumulation of ROS and limits ion toxicity. (4) Antioxidative enzymes are activated by increased
cellular ROS, and Si may further increase their activity. These enzymes scavenge ROS within the cell,
thus protecting it against oxidative damage. (5) Si deposited outside the cell reduces evapotranspiration,
protecting the plant against water stress. After Thorne et al., (2020)

Thorne et al., (2020) stated that salinity affects around 20% of all arable land while an even larger
area suffers from recurrent drought. Together these stresses suppress global crop production by as much
as 50% and their impacts are predicted to be exacerbated by climate change. Infrastructure and
management practices can mitigate these detrimental impacts, but are costly. Crop breeding for improved
tolerance has had some success but is progressing slowly and is not keeping pace with climate change.
In contrast, Silicon (Si) is known to improve plant tolerance to a range of stresses and could provide a
sustainable, rapid and cost-effective mitigation method. The exact mechanisms are still under debate but
it appears Si can relieve salt stress via accumulation in the root apoplast where it reduces “bypass flow
of ions to the shoot. Si-dependent drought relief has been linked to lowered root hydraulic conductance
and reduction of water loss through transpiration. However, many alternative mechanisms may play a
role such as altered gene expression and increased accumulation of compatible solutes. Si can reduce
oxidative damage that occurs under stress conditions through increased antioxidative enzymes while Si-
improved photosynthesis has also been reported. Si fertilizer can be produced relatively cheaply and to
assess its economic viability to improve crop stress tolerance we present a cost-benefit analysis. It
suggests that Si fertilization may be beneficial in many agronomic settings but may be beyond the means
of smallholder farmers in developing countries. Si application may also have disadvantages, such as
increased soil pH, less efficient conversion of crops into biofuel and reduced digestibility of animal
fodder. These issues may hamper uptake of Si fertilization as a routine agronomic practice. Here, we
critically evaluate recent literature, quantifying the most significant physiological changes associated
with Si in plants under drought and salinity stress. Analyses show that metrics associated with
photosynthesis, water balance and oxidative stress all improve when Si is present during plant exposure
to salinity and drought. We further conclude that most of these changes can be explained by apoplastic
roles of Si while there is yet little evidence to support biochemical roles of this element.
In addition, an excessively high concentration of salt ions in the soil will a_ect the absorption of
other elements (such as nitrogen and calcium) by plants, resulting in ion imbalance, whereas Si has been
found to increase the concentration of macroelements, such as Ca, P, and Mg, and microelements, such
as B, Fe, Zn, and Mn, in many kinds of plants Zhu et al., (2014). Aquaporin has been reported to play

328
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27
important roles in nutrient homeostasis and recent researches suggested that Si could improve plant
water content through regulating the activities of root aquaporins.
5.2.6. Potential Interaction between Silicon and Ionic Stress Signaling Pathways
Under salt stress conditions, rapidly sensing excess Na+ signal is a prerequisite for initiating the
reestablishment of cellular ionic homeostasis Yang and Guo (2018). Generally, salt treatment activates
the salt overly sensitive (SOS) signaling pathway within a short time period, which is crucial for the
regulation of plant ionic homeostasis through extruding Na+ into the apoplast Yang and Guo (2018)
Fig. (40).

Fig. 40: Illustrates ion homeostasis in response to salt stress. In response to salinity stress, SOS pathway
(enabling Na+ efflux), vacuolar sequestration of Na+ and K+ inclusion play an important role in inducing
salt tolerance in the cells under stress. The SOS pathway isa cascade that involves SOS 1, 2 and3. SOS3
is itself a Na+H+ antiporter that helps in Na+ exclusion from cells under stress. High extracellular Na+
ion concentration leads to calcium-dependent activation of SOS3. SOS2 increases the nuclear
translation ofSOS1genes and extrudes Na+ from the cells. Tonoplast-associated transporters such as
NHX, CHX and VATP-ases are required for vacuolar sequestration of Na+ ions. Plasma membrane-
associated transporters KUP1, HAK5and CHX17 cause an increase in intracellular concentration of K+
that is required for tolerance induction during increased cytosolic Na+ concentrations. After Amina et
al., (2021).

Amina et al., (2021) stated that, sodium chloride is the most important salt responsible for
inducing salt stress by disrupting the osmotic potential. Due to various innate mechanisms, plants adapt
to the sodic niche around them. Genes and transcription factors regulating ion transport and exclusion
such as salt overly sensitive (SOS), Na+/H+ exchangers (NHXs), high sodium affinity trans-porter
(HKT) and plasma membrane protein (PMP) are activated during salinity stress and help in alleviating
cells of ion toxicity. For salt tolerance in plants, signal transduction and gene expression is regulated
via transcription factors such as NAM (no apical meristem), ATAF (Arabidopsis transcription
activation factor), CUC (cup-shaped cotyledon), Apetala2/ethylene responsive factor (AP2/ERF), W-
box binding factor (WRKY) and basic Leucine zipper domain (bZIP). Cross talk between all these
transcription factors and genes aid in developing the tolerance mechanisms adopted by plants against
salt stress. These genes and transcription factors regulate the movement of ions out of the cells by
opening various membrane ion channels. Mutants or knockouts of all these genes are known to be less
salt-tolerant compared to wild types. Using novel molecular techniques such as analysis of genome,
transcriptome, ionome and meta bolome of a plant, can help in expanding the understanding of salt
tolerance mechanism in plants. In this review, we discuss the genes responsible for imparting salt
tolerance under salinity stress through trans-port dynamics of ion balance and need to integrate high-
through put molecular biology techniques to delineate the issue.
High-affinity K+ channel (HKT1) is a key determinant of plant salinity tolerance that may
function to mediate Na+ influx across the plasma membrane and decrease Na+ accumulation in the
shoot, thus protecting leaves from Na+ toxicity and improving salt tolerance Yang and Guo, (2018).
Until now, little is known about the effect of Si on putatively SOS1-mediated NaCl efflux. More

329
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

recently, Bosnic et al., (2018) proposed that Si decreased Na accumulation in both root apex and cortex
of maize. Meanwhile, Si addition allocated more Na+ to the leaves via the xylem through upregulating
ZmSOS1 and ZmSOS2 in the root cortex, but down regulating ZmHKT1. Furthermore, Si enhanced
sequestration of Na+ into the vacuoles by upregulating ZmNHX, and thus decreased Na+ accumulation
in the chloroplasts. This study firstly experimentally demonstrated the direct effect of Si on the
expression of SOS and HTK genes. However, the deeper mechanism, such as the detailed regulation
mechanisms of Si on SOS signaling pathways, remains obscure. Moreover, it would be interesting to
dissect the interaction between Si and other salt stress sensors (e.g., Mitogen-activated protein kinase
(MAPK)) involved in salt-induced stress signaling in plants.

5.2.7. Participation of Polyamine in Silicon-Mediated Ion Homeostasis

Recent studies suggested that the effects of Si on the levels of ions, particularly Na+ and K+,
during salinity stress might be associated with the regulation of polyamine metabolism. Polyamines are
small aliphatic polycations that are widely distributed in prokaryotic and eukaryotic cells. In higher
plants, putrescine, spermidine, and spermine are the most abundant polyamines, they can be present in
different forms, including free, insoluble-bound, and soluble conjugated Yin et al., (2019). During
salinity stress, polyamines can regulate the transport of Na+ and K+ in plants through nonselective ion
channels Zhao et al., (2007), recently, the regulatory effects of Si on polyamine metabolism under salt
stress have been reported in cucumber and sorghum. In sorghum, Yin et al., (2016) found that the
addition of Si could increase free and total polyamine levels and decrease Na+ accumulation. Moreover,
Si application balanced the metabolism of polyamines and ethylene through inhibiting the level of 1-
aminocyclopropane-1-1-carboxylic acid (ACC), an important ethylene precursor, to mitigate salt stress.
Wang et al., (2015) also found that Si had some regulatory effects on polyamine levels (increasing the
concentrations of free and conjugated putrescine and free spermidine, but decreasing the concentration
of conjugated spermidine), as well as alleviating K+/Na+ homeostasis in salt-stressed cucumber,
suggesting the involvement of polyamine in Si’s reduction of ion toxicity. However, it is still hard to
draw the conclusion that Si could mediate the K+/Na+ homeostasis through regulating polyamines
content according to these studies, because under certain conditions, polyamines will not decrease, but
promote K+ efflux under salinity stress Yin et al., (2016). Therefore, more evidence is required to prove
how Si regulates polyamine metabolism and determine under which conditions (e.g., NaCl
concentration, stress duration, and seedling age) that Si could regulate polyamine metabolism to balance
the K+/Na+ homeostasis. Taken together, these studies show that the Si addition can decrease Na+
absorption in the root and/or transport to shoot to alleviate the damage caused by salinity stress.
However, this mechanism varies between species and varieties and the influence of Si on Na
partitioning at the cell, tissue, and organelle levels is still unclear. Moreover, the exact mechanisms of
how Si regulates transcription of various mineral transporter genes remain unclear. One may speculate
that the regulation of Na+ absorption by Si in different species might be affected by the Si absorption
ability of roots. In addition, the relationship of SiO2 – plant cell wall has been well documented in Si
accumulators, including monocots and pteridophytes Guerriero, et al., (2016). Coskun et al., (2019)
proposed an apoplastic obstruction model to explain beneficial effects of Si in plants, which proved
guidance for further study. Nevertheless, the role of Si-induced modifications in the mechanical
properties and composition of the cell wall in decreasing Na+ uptake and/or transport is largely
unknown. On the other hand, some recent studies have shown that interfering with Na+ uptake and
assimilation is not the only mechanism by which Si alleviates salinity stress damage in plants. For
example, in tomato, Romero-Aranda et al., (2006) found that addition of Si did not decrease Na+ and
Cl- concentrations in leaves, but increased the tissue water content to dilute the salt ions that were
absorbed. Chen et al., (2014) carried out a study in wheat, and found that Si application could alleviate
both ion toxicity and osmotic stress caused by salinity stress, with the alleviative effect of the latter
being more significant. Zhu et al., (2015) reported that the decrease in Na+ levels in two cucumber
cultivars was not the main mechanism by which Si alleviated salinity stress damage. Apart from ionic
stress upon long-term salinity exposure, osmotic effect upon short-term salinity exposure reduces the
ability of the plant to take up water and inhibit growth rate Yang and Guo, (2018). However, current
studies on Si’s alleviation of osmotic stress caused by salinity stress are limited; this is not conducive
to further explore the alleviation mechanisms of Si under salt stress.

330
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

5. 2.8. Silicon and plant water balance under salinity stress

The presence of salt in the external soil environment reduces the ability of plants to extract water
and these results in physiological drought, which is the major stress affecting plant growth during short-
term salinity stress. However, previous studies on Si’s alleviation of salinity stress have mostly focused
on the alleviation of ionic stress, and there are relatively few integrated studies on the regulatory effect
of Si on water absorption and transport.

5.2.9. Water Relation

Earlier studies showed that Si could decrease the transpiration rate through its deposition on the
surface of leaves, thereby decreasing water loss through transpiration and maintaining relative higher
water content in plants Matoh et al., (1986). However, Si application does not always result in decreased
plant transpiration. For example, Gong et al., (2006) and Zhu et al., (2015) found that Si addition
increased the leaf transpiration rate of salt-stressed rice and cucumber seedlings, suggesting a possible
role of Si in regulating water uptake in plants. The root system is the first tissue that perceives salt stress
and salinity affects the root architecture Yang and Guo, (2018). Recent studies have revealed that Si
addition under salinity stress can increase water content in plants through increasing root water
absorption Yin et al., (2019), Wang et al., (2015). In tomato, Li et al., (2015) found that Si promoted
root growth and root hydraulic conductance, thereby increasing root water uptake and further improving
leaf water content. In sorghum, Liu et al., (2015) reported that Si could increase root hydraulic
conductance and water absorption by regulating the activity of aquaporins under salt stress Fig. (41).

Fig. 41: Illustrates impact of abiotic stress on various aspects of plant growth and defense mechanisms
evoked by application of Si. After Mir etal (2022)

After Mir et al., (2022) reported that crop plants might grow well in the absence of Si, although
in a few plants, such as rice and horsetail, the absence of Si may make them vulnerable to fungal
infections Law and Exley, (2011). Si has been reported to play numerous roles in mitigating abiotic
stress conditions Alamri et al., (2020), Salim et al., (2021). For instance, Si mediates diverse strategies
to sequester the metal ions by modulating soil pH, metal speciation, precipitation, and
compartmentalization Debona et al., (2017). Recent trends have proved the evolution of Si-based
fertilizers to impart growth and developmental effects of crop plants, such as enhancing photosynthesis
and regulating electrolytic leakage under stress conditions Chen et al., (2011). For example, Si enhances
photosynthesis in mango trees and increases water and nutrient uptake under abiotic stress conditions
Santos et al., (2014). Si is found in almost all the plants in variable amounts, imparting varying
physiological effects Cooke and Leishman, (2011). Apart from its critical role in stress tolerance
imposed by excess salt and drought, uptake of Si results in enhanced mechanical support to shoots and
leaf blades Zhu et al., (2019a). Numerous reports reveal the application of Si in mitigating abiotic and

331
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

biotic stresses in various plant species Zargar et al., (2019); Gou et al., (2020). Moreover, Si plays a
vital role in ameliorating metal toxicity in several crop plants Singh et al., (2019); Wu et al., (2019).
Moreover, Si helps to mitigate metal ion stresses like that of aluminum (Al) and manganese (Mn) stress
in crop plants Tripathi et al., (2016). Water uptake through aquaporins and root hydraulic conductance
is upregulated by administering exogenous Si Liu et al., (2015).
In these studies, an elevation in leaf water status facilitated the maintenance of stomata in an open
state, thereby increasing CO2 uptake and thus photosynthetic rate. Zhu et al., (2015) proposed that Si
increased the expression of the main plasma membrane aquaporins in two-cucumber cultivars ‘JinYou
1’ and ‘JinChun 5’, thus increasing the root hydraulic conductance under salt stress. This, together with
an increased stem hydraulic conductance with Si addition, allows for an increase in leaf water content
and finally dilutes the absorbed salt ions. However, it is still unclear whether the increase in hydraulic
conductance is due to an improvement in the root system structure. Moreover, the effect of silicon on
the capacity of the main plasma membrane aquaporins still needs to be confirmed using a molecular
biology approach. Wang et al., (2015) reported similar results in another cucumber cultivar, ‘JinChun
10’. Nevertheless, Si application not only improved the water content in the leaves of ‘JinChun 10’, it
also significantly decreased the Na+ content and increased the K+ content in leaves, while it was less
likely that Si was actively involved in reducing Na+ accumulation in ‘JinYou 1’ and ‘JinChun 5’. These
differences might be related to different cucumber cultivars (salt stress-tolerant or -sensitive), salinity
stress duration, and salt concentrations used in the two studies. Previous studies found that Si deposition
on cell walls increases the affinity of xylem vessels for water, thereby affecting water transport
capabilities in the xylem Gao et al., (2005). However, Liu, et al. (2014), pointed out that stem water
transport is not the major limiting factor affecting water transport during water-deficit stress in sorghum.
Therefore, further studies are required to determine the effects of Si on different transport vessel
structures in plants. In addition, the aquaporin inhibitor, mercury chloride (HgCl2) has been used in
some studies to prove that Si increases root hydraulic conductance through regulating expression of
root AQPs Zhu et al., (2015);Yang and Guo, (2018) and Liu et al., (2014). In salt-stressed sorghum, Si
treatment could significantly increase the transpiration rate, whereas the HgCl2 treatment incensing the
effect of Si in transpiration rate; after recovery induced by dithiothreitol (DTT); however the
transpiration rate was higher in Na+Na2SiO3-9H2O treated seedlings than Na- treated seedlings Liu et
al., (2014), However, it is worth noting that Hg2+ can act as an inhibitor of both aquaporin and K+
channels. K+ is an important compatible solute that can regulate water absorption and transport in the
root system Coskun et al., (2012); Dolan and Davies, (2004). Besides, not all plant aquaporins are
sensitive to Hg, and Hg could have other secondary effects as well Aroca et al., (2011). The mechanism
by which Si increases root water uptake requires more evidence.

5.2.10. Osmotic Regulation

Osmoregulation is a primary adaptive strategy of plants at the cellular level to derogate the effects
of salinity-induced osmotic stress. Salinity stress activates the salt-mediated osmotic stress pathways
that induce the synthesis and accumulation of compatible osmolytes (e.g., proline, betaine, and soluble
sugars) to increase the osmoregulatory functions of plants Parida, and Das, (2005), Gupta and Huang
(2014). Some studies have shown that Si participates in regulating the accumulation of osmoregulatory
substances in plants. Examples of this include sorghum and wheat, where researchers found that the
addition of Si could significantly alter the soluble sugar and proline content in plants Yin, etal (2013).
Sattar, etal. (2017). In cucumber, Na+Na2SiO3.9H2O treatment could increase the accumulation of
soluble sugars (mainly sucrose and glucose) and decrease the osmotic potential of xylem sap in the root
system compared with Na treatment, thus contributing to the promotion of root water uptake Zhu, et al.
(2016). However, this regulatory effect of Si exhibits intercultivar differences, and whether Si
participates in enhancing assimilate transport to provide more energy storage in the roots needs to be
experimentally proved. Moreover, carbohydrates such as sugars (e.g., glucose, fructose, and fructans)
are involved not only in osmoprotection, but also in carbon storage and scavenging of ROS Zhu et al.
(2016).

5.2.11 Silicon and Reactive Oxygen Species in Responses to Salt Stress

During salinity stress, one of the immediate responses of plants is overproduction of reactive
oxygen species (ROS), such as hydrogen peroxide (H2O2), superoxide (O2-), and hydroxyl radicals

332
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

(OH.). The increase of ROS will cause oxidative damage to membranes and organelles Liu, etal. (2015).
The antioxidant systems include enzymatic and nonenzymatic antioxidants. In plants, enzymatic
antioxidants mainly include catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), and
ascorbate peroxidase (APX). Nonenzymatic antioxidants mainly include vitamin E, ascorbic acid, and
glutathione reductase (GR) Choudhury, et al. (2017). Previous studies have shown that Si could improve
ROS scavenging ability by regulating the activities/contents of enzymatic/nonenzymatic antioxidants
in plants, and the regulatory effect is different depending on plant species. For example, in barley, Si
could increase the activity of CAT, SOD, and GR, but had no effect on the APX activity Liang, et al.
(2003). In cucumber, the addition of exogenous Si could increase the activities of APX, SOD, GPX,
and GR, but had no effects on the CAT activity Zhu, et al. (2004). In sorghum, Si application has been
proposed to reduce the accumulation of H2O2, which plays a negative role in regulating the activity of
aquaporin to enhance aquaporin activity, and thus increase water uptake Liu, et al. (2015). Similar
results were also found in okra (Abelmoschus esculentus) Abbas et al. (2015), grapes (Vitis vinifera L.)
Soylemezoglu, et al. (2009), wheat Tuna, et al., (2008), tomato Li et al., (2015), and rice Abdel-Haliem
et al. (2017). Moreover, the regulatory pattern is different depending upon plant species and Si intensity.
Application of Si gradually enhanced AsA-GSH particularly in two rice cultivars differing in salt
tolerance. Such effect were more pronounced upon Si administration in the sensitive cultivar Das, et al.
(2018). One study on Glycyrrhiza uralensis showed that the exogenous addition of 1, 2, 4, and 6 mM
Si could significantly increase POD activity and reduce malondialdehyde (MDA) concentrations
compared to salinity stress alone. However, the SOD activity significantly increased when 4 mM Si
was used Li, et al. (2016). These results showed that even though the regulatory effects of Si on
antioxidant defense systems under salinity stress can vary with plant species, treatment duration,
treatment concentration, and growth conditions, overall, Si can decrease the accumulation of ROS
through regulating both enzymatic and nonenzymatic antioxidants.

5.2.12. The regulatory effect of silicon on genes expression in responses to salt stress
Owing to the advancement of molecular genetics and genome wide technologies, significant
research advances have been made to enhance our understanding of the involvement of Si in increasing
stress tolerance. Kim, et al. (2014) reported that Si application significantly upregulated the expression
of genes associated with ABA synthesis (zeaxanthin epoxidase (ZEP) and 9-cis-epoxycarotenoid
dioxygenase (NCED1 and NCED4)) in rice after 6 and 12 h of the NaCl treatment, but decreased the
expression of these genes after 24 h of treatment. In sorghum and cucumber, Si application increased
the plasma membrane aquaporin expression in the roots to increase the hydraulic conductance and water
uptake ability Yang and Guo (2018), Liu, et al. (2014),. In tobacco, Liang, et al. (2015) discovered the
cooperation between Si and ethylene signaling pathway. They found that Si application rapidly
upregulated the expression of crucial ethylene biosynthesis genes, 1-aminocyclopropane-1-carboxylic
acid oxidase (ACO) and 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS), which
increased ethylene levels and regulated plant responses to salinity stress. However, when ethylene was
absent, Si did not increase the tolerance of cells to salinity stress, but promoted the production of
hydrogen peroxide, leading to cell death. Competition is considered to exist between ethylene and
polyamines since they share a common precursor, S-adenosyl-L-methionine (SAM).

5.2.13. Impacts of Si in Alleviating Salt-Induced Oxidative Damage

Salinity is one of the most important environmental factors limiting crop production in arid and
semi-arid regions. Salinization of land and water resources is a threat for sustainability of irrigated
agriculture Qureshi, et al., (2007). They reported that half of the irrigated area of Iran falls under
different types of salt affected soils and average yield losses may be as high as approximately 50%.
Following primary effects of salt stress, secondary stresses such as oxidative damage may occur.
Oxidative damage occurs by accumulation of reactive oxygen species (ROS) that cause lipid and protein
oxidation and eventually leads to cell death Molassiotis et al., (2006). The antioxidant defence system
in the plant cell includes both enzymatic antioxidants such as APX (EC1.11.1.11), CAT (EC1.11.1.6),
SOD (EC1.15.1.1), POX (EC 1.11.1.7), and GR (EC 1.6.4.2) and some non-enzymatic antioxidants
such as ascorbate, glutathione and αtocopherol Ashraf and Harris (2004); Gunes, et al., (2007); Ashraf,
(2009).

333
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Salinity is a major abiotic stress that limits the growth and yield of agricultural and horticultural
crops worldwide. Primarily, salinity hampers the osmotic balance in plants by affecting the
electrochemical gradients and vascular transportation of solutes Marschner (1995). In higher plants, salt
stress leads to several physiological and metabolic modulations such as retardation of photosynthesis,
ion toxicity, oxidative burst, and nutrient imbalance Allakhverdiev, etal. (2000), Kosova, etal. (2011).
In addition, higher accumulation of Na+ and Cl− ions during saline conditions hinders the uptake of
essential nutrients Agarie, etal. (1998).Furthermore, salinity accelerates the production of harmful
reactive oxygen species (ROS) that cause oxidative damage to proteins, lipids, and nucleic acids by
affecting normal cellular metabolism Zhu,etal.(2004). Hence, an alternative strategy of silicon (Si)
supplementation to overcome the negative effects of salinity in plants can be considered as a valuable
approach. Silicon is the second most abundant element in the Earth’s crust, covering 27.70% of the
lithosphere. Numerous plant biologists have extensively studied the essential roles of Si in plant systems
for several years, but by definition, Si is considered as a “quasi-essential” or nonessential element for
plants, because most plant species can complete their life cycle without it Arnon and Stout (1939).
However, there are several hypotheses concerning the physiological functions of Si in monocots and
dicots. Under abiotic stress like salinity, Si application resulted in the alleviation of stress and
enhancement of plant growth Soundararajan, etal. (2014), Li, et al. (2015). During salt stress, the
apoplastic transport of Na+ and Cl− ions was decreased by Si deposition Shi, et al. (2013), Gong, et al.
(2005). According to Zhu .and Gong (2014), the mechanisms behind silicon-mediated alleviation of salt
stress include the following aspects: (a) maintenance of optimal water content; (b) enhancement of
photosynthesis and curbing transpiration rate; (c) limiting oxidative stress by alleviating ion toxicity;
and (d) biosynthetic regulation of solutes and plant hormones. In line with other researchers, Al-
aghabary, et al. (2005) observed increased activities of antioxidant enzymes and enhanced
photochemical efficiency of PSII under salt stress. Although the beneficial effects of Si against abiotic
stresses are evident from previous reports, to date there is a lack of understanding of the molecular
regulation of Si mediated stress tolerance. In order to gain a deeper insight into Si induced salt tolerance
in pepper plants, proteomic analysis based on two-dimensional gel electrophoresis- (2DE-) mass
spectrometry (MS) has been employed in the present study. Moreover, proteomic strategies are
considered the best molecular approach to study the dynamics of proteins, particularly the response of
Si in a stressed environment Rahman, et al. (2015), Campos, et al. (2003). Therefore, to our knowledge,
for the first time, the current study has attempted to investigate the effect of Si on the growth,
physiology, antioxidant enzyme activities, nutrient content, and protein expression in C. annuum under
salinity stress.
Application of Si suggested as an alternative approach to alleviate salinity stress in crops (Liang
et al., 2007). However, Si content of the plant varies greatly with the plant species, ranging from 0.1 to
10.0% of dry weight Takahashi et al., (1990). Si, increases root activity, K uptake, reduction of Na
uptake, improvement of membrane permeability and anti-oxidative activity (Liang et al., 2007).
Sorghum is one of the most important crops of arid and semi-arid regions. It is moderately tolerant to
salinity and can grow well in saline soils Maas et al., (1986). However, at higher levels of salinity,
considerable reduction in its growth takes place; therefore, improvement of its salinity tolerance by any
means is a great challenge for plant scientists. Although a variety of strategies are currently in vogue to
counteract the salinity problem, application of Si considered as one of the convenient and cost-effective
approaches of overcoming the salinity menace.
Most recently, studies suggested that Si might participate in regulating the antioxidant defense
system and relieving oxidative stress through enhanced endogenous polyamine accumulation (mainly
spermidine and spermine) Yin et al., (2019). The interactive effects between Si and exogenous
substances including mineral element and plant hormone have been reported in several species. In
chickpea, Garg and Bhandari, (2016) evaluated the individual and cumulative effect of Si and arbuscular
mycorrhiza (AM) under salinity stress conditions. The results showed that mycorrhiza significant
improved Si uptake and Si addition, alone or combined with mycorrhizal inoculation, increased the
activities of antioxidant enzymes, such as SOD, CAT, and GPOX, and decreased ROS accumulation
under salinity stress. Study of the combination effect of exogenous application of Si and/or other
substances like beneficial soil microorganisms and elements in alleviating biotic/abiotic stresses may
facilitate the use of Si in more plant species, especially for Si excluders. Potassium (K) is a macro-
element that has been reported to ameliorate adverse effects of salt stress in many species Bybordi,

334
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

(2014). A great interactive effect between Si and K were reported in improving antioxidant enzyme
activity, photosynthetic rate, K uptake, and yield Lotfi, (2015). Selenium (Se), an important
micronutrient in animals and humans, functions as a beneficial element in some crops. Studies proved
that the combined application of Si and Se was more effective than Si alone in alleviating the toxic
effects of salt stress on wheat seedlings through increasing antioxidant enzyme activity and
accumulation of osmoprotectants like proline and soluble sugar Liu et al., (2015). Salicylic acid (SA),
a plant hormone, is an important signal molecule for modulating plant responses to environmental
stresses. Application of salicylic acid and Si has been reported to improve seed quality of mung bean
under salinity Lotfi and Ghassemi-Golezani, (2015). Future work is needed to investigate the
interactions between silicon and other substance and their coupled response/functionality under salt
stress conditions. Although studies have unraveled the regulatory effect of Si in ROS scavenging, many
questions related to its mode of regulation remain unanswered. First and most important, whether this
was a primary or a secondary effect of Si on ROS detoxifying proteins (e.g., SOD, APX, CAT, and
GPX), and antioxidants such as ascorbic acid and glutathione (GSH) remains unclear from these studies.
In the review of Coskun et al., (2019) proposed that there are no biochemical roles for Si (OH)4, an
uncharged and unreactive molecule, in terms of interactions with enzymes or other intracellular
constituents. Therefore, more studies are needed to examine the possible promotion effects of Si on the
activities of antioxidant enzymes of plants under stress conditions. Second, metabolic and signaling
ROS are shown to accumulate in the different compartments of the cells, mainly chloroplast,
mitochondria, peroxisome, and apoplast. Moreover, each set of different biotic and abiotic stress
conditions will result in abiotic stress-specific ROS signaling AO et al., (2005), Sewelam et al., (2016).
If Si plays an active role in regulating ROS scavenging, it should be further specified when, where, and
how (through regulating stress acclimation proteins and enzymes or expressions of genes involved in
managing the level of ROS?). Third, it is worth noting that ROS is not always damaging. If cells
maintain high enough energy reserves to detoxify ROS, they primarily function as signal transduction
molecules that regulate different pathways during plant growth as well as the acclimation of plants to
stress Sah et al., (2016); Choudhury et al., (2017). How this conflict of ROS production (metabolically
or for signaling purposes) and ROS scavenging is resolved in plants is largely unknown, but it is mainly
controlled by the ROS gene network Mittler et al., (2004). Taking the complex nature of the ROS gene
network and its function in plant signal transduction pathways into consideration, the cellular/molecular
mechanisms controlling Si-induced/eliminated ROS signaling need to be elucidated.

6. Toxicity Symptoms related to Ionic and Nutritional Balance in Plants

Saline solutions impose ionic and osmotic stress in plants. The effects of this stress can be
observed at different levels. In sensitive plants, the growth of aerial parts and roots is rapidly reduced.
Reduction phenomenon appears to be independent of the tissue Na+ concentration but would rather be
a response to the osmolarity of the culture medium Munns, (2002). The specific toxicity of Na+ ions is
related to the accumulation of these ions in the leaf tissues and leads to necrosis of the aged leaves.
Generally, this necrosis begins with the tip and the edges to finally invade the entire leaf. The reduction
in growth is due to a reduction in leaf life, and thus there will be a reduction in growth and productivity
Munns, (1993) & (2002). In saline soils, Na+ ions induce deficiency in other elements Silberbush et al.,
(2005). The effects of Na+ are also the result of deficiency in other nutrients and interactions with other
environmental factors, such as drought, which increase the problems of Na+ toxicity. The excess of Na+
ions inhibits the uptake of other nutrients either by competition at the sites of the root cell plasma
membrane transporters or by inhibition of root growth by an osmotic effect. Thus, the absorption of
water and the limitation of the nutrients essential for the growth and the development of the
microorganisms of the soil can be inhibited. Leaves are more sensitive to Na+ ions than roots because
these ions accumulate more in the aerial parts than in the roots. These can regulate the concentration of
Na+ ions by their export either to the aerial parts or to the ground. The metabolic toxicity of Na+ is
mainly related to its competition with K+ at sites essential for cell function. Thus, more than 50 enzymes
are activated by K+ ions; Na+ ions cannot replace K+ in these functions Bhandal and Malik, (1988);
Tang et al., (2015); Gu et al., (2016). For that, a high concentration of Na+ can affect the functioning
or the synthesis of several enzymes. In addition, protein synthesis requires high K+ concentrations for
tRNA binding on ribosomes Blaha et al., (2000) and probably for other ribosome functions Wyn Jones
et al., (1979). The disruption of protein synthesis by the high concentration of Na+ represents the major

335
 Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

toxic effect of Na+ ions. Osmotic stress could occur following an increase in Na+ concentration at leaf
apoplasm Oertli, (1968). This result was verified by microanalyses (R-X) of Na+ concentration in
apoplasm of rice leaves Flowers et al., (1991). The presence of high concentrations of Na+ in the cells
allows the plant to maintain its water potential lower than that of the soil to maintain its turgor and water
absorption capacity. This leads to an increase in osmotic concentration by absorption of solutes either
from the soil or by synthesis of compatible solutes. The former, usually Na+ and Cl- , are toxic, while
the latter are compatible but energetically expensive for the plant.

6.1. Effects of NPs on plant under salinity stress

Nanoparticles enter the plant system by several routes, mainly through roots and leaves NPs
interact with plants at cellular and subcellular levels after entry, promoting changes in morphological,
biochemical and physiological and molecular states Khan et al., (2019b). These interactions may be
positive or negative, depending on the nature of the NPs and the plant species Fig. (42).

Fig. 42: Illustrates the interactions of NPs on plant under salinity stress at physiological, biochemical
and molecular levels. After Etesami et al., (2021)

The chemical nature, reactivity, size, and specifically concentration of NPs in or on the plant
could determine NPs’ effects on plant systems Ma et al., (2010), Paramo et al., (2020); Tripathi et al.,
(2017a); Zulfiqar and Ashraf, (2021). Available evidence has shown that different NPs can promote
salinity-stressed plant growth and development Ali et al., (2021); Aslani et al., (2014); Zulfiqar and
Ashraf (2021) at concentrations below certain limits by various known mechanisms. These studies were
mostly performed under artificial treatment conditions such as plate growth medium and hydrophobic
or pot conditions. To understand the impact of NPs on plant growth, we discuss the positive effects of
NPs to improve plant salinity stress tolerance.

6.2. Trace Elements and Nanoparticles

During the last few years, rapid advances of nanotechnology are associated with release of
different types of nanoparticles. Some of them may be accumulated in soil or natural environment with
negative effects on biota Alharby et al., (2016), Yassen et al., (2017). The authors have reported the
detrimental effects of nanoparticles (usually at relatively high concentration) on plant health. However,
there is evidence about the positive effects of nanoparticles, which is achieved at relatively low
concentrations. This provides the scope for possible agricultural applications of nanoparticles Siddiqui
et al., (2014), Siddiqui and Al-Whaibi, (2014); Askary et al., (2016). One of the promising ways is the
use of nanofertilizers. Applying the nutrients in the form of nanoparticles improves the nutrient use
efficiency, with low risk of toxicity for soil microbiota and roots Fig. (43).

336
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 43: Schematic diagram illustrating the potential role of nanoparticles (NPs) in alleviating the toxic
effects of trace elements in plants through several potential mechanisms. After Rahman et al., (2022)

Rahman et al., (2022) reported that using of nanoparticles (NPs) as nano-fertilizers or nano-
pesticides is gaining popularity worldwide. The NPs-mediated fertilizers encourage the balanced
availability of essential nutrients to plants compared to traditional fertilizers, especially in the presence
of excessive amounts of TEs. Moreover, NPs could reduce and/or restrict the bioavailability of TEs to
plants due to their high sorption ability. They stated that the potential influence of NPs on plant
physiological attributes, mineral absorption, and TEs sorption, accumulation, and translocation. It also
unveils the NPs-mediated TE scavenging-mechanisms at plant and soil interface. NPs immobilized TEs
in soil solution effectively by altering the speciation of TEs and modifying the physiological,
biochemical, and biological properties of soil. In plants, NPs inhibit the transfer of TEs from roots to
shoots by inducing structural modifications, altering gene transcription, and strengthening antioxidant
defense mechanisms. On the other hand, the mechanisms underpinning NPs-mediated TEs absorption
and cytotoxicity mitigation differ depending on the NPs type, distribution strategy, duration of NP
exposure, and plants (e.g., types, varieties, and growth rate), NPs may bring new possibilities for
resolving the issue of TE cytotoxicity in crops, which may also assist in reducing the threats to the
human dietary system. Moreover, such a way of application reduces the frequency of the application
and prevents the risk of over dosage. Hence, the potential of nanotechnology to support the sustainable
farming is high, including developing countries Naderi and Danesh-Shahraki, (2013); Yassen et al.,
(2017). The second way of application relates to exogenous use of trace elements and nanoparticles to
mitigate stress effects by influencing some specific plant processes Zhao, et al. (2012); Rico, et al.
(2013); Rossi, et al. (2016). For example, the zinc treatment led to lower MDA and H2O2 concentration
in tissues in the experimental plants under salt stress, which was associated with upregulation of total
APX, CAT, POD, and PPO activities under salt stress Weisany et al., (2012); El-Bassiouny et al.,
(2020). Decreasing of lipid peroxidation and proline contents under salinity by applying Fe2O3NPs has
been found in the peppermint plants. The appropriate concentration of iron nanoparticles can be used
for stress resistance of the peppermint Askary et al., (2017). Fathi et al., (2017) and Soliman et al.,
(2015) haves demonstrated the positive influence of Zn and Fe and their NPs in stress conditions.
Nanoparticles were more efficient than other tested forms of these micronutrients Fig. (44).

337
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 44: Illustrates nanotechnology-based agriculturally important nano fertilizers increase agronomic
productivity, efficiency, and reduce environmental stress. Efficient utilization of nanotechnology in
agriculture for future sustainability. After Mittal et al., (2020)

Mittal et al., (2020) stated that it is an urgent requirement to satisfy the nutritional demands of
the rapidly growing global population. Using conventional farming, nearly one third of crops is
damaged, mainly due to pest infestation, microbial attacks, natural disasters, poor soil quality, and lesser
nutrient availability. More innovative technologies are immediately required to overcome these issues.
In this regard, nanotechnology has contributed to the agro technological revolution that has imminent
potential to reform the resilient agricultural system while promising food security. Therefore,
nanoparticles are becoming a new-age material to transform modern agricultural practices. The varieties
of nanoparticle-based formulations, including nano-sized pesticides, herbicides, fungicides, fertilizers,
and sensors, have been widely investigated for plant health management and soil improvement. In-
depth understanding of plant and nanomaterial interactions opens new avenues toward improving crop
practices through increased properties such as disease resistance, crop yield, and nutrient utilization,
could benefit productivity and food security in future
It can be caused by their size, shape, distribution, and other physical characteristics. Latef et al.,
(2017) reported that priming of seeds with ZNPs is a useful strategy to increase the salt tolerance of
lupine plants. The most efficient was concentration of ZnO NPs 60 mg L−1. El-Bassiouny et al., (2020)
reported that, seed-priming with ZnO-NPs or ZnO-bulk in the presence and absent of Arbuscular
mycorrhiza (AM) fungi increased the levels of organic solutes (TSS, proline and FAA) in two wheat
cultivars under salinity stress. Nano-ZnO (10mg/l) in the presence of AM was the most effective
treatments on both wheat cultivars. Moreover, application of ZnO-NPs is the main defense mechanism,
as a possible initiator of oxidative stress of the plant via enhanced the secondary metabolism is mainly
due to the increase in phenolic compounds and antioxidant enzyme activities Fig.(45). It has been also
shown that exogenous nanoparticles such as cerium oxide nanoparticles (CeO2-NPs) positively
influence plant growth and production under normal growth conditions. Depending on soil moisture
content, CeO2-NPs supported photosynthesis, which led to increase of water use efficiency (WUE),
especially in water-restricted conditions Cao et al., (2017). Under salinity, it was found that CeO2-NPs
application led to improved plant growth and physiological responses of canola, improving the salt
stress responses. However, the stress effects were not fully alleviated by CeO2-NPs Rossi et al., (2016).

338
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 45: Mechanism of alleviation of oxidative stress in plant by nanomaterials. Amendment of

Nanomaterials induces Nitric oxide (NO) production that initiate signal and trigger generation of
enzymatic and non-enzymatic antioxidant superoxide dismutase (SOD), guaiacol peroxidase (GPX),
catalase (CAT) and phenols that scavenge ROS (O2 −·, H2O2, OH−) generated in different cell
organelles due to abiotic stress. SOD dismutate superoxide radical (O2 −·) into hydrogen peroxide
(H2O2), which on action of CAT and GPX converted into water molecule (H2O) and molecular oxygen
(O2), thereby reducing ROS concentration and oxidative damage to proteins, lipids and nucleic acid
After Sachdev and Ahmad, (2021).

Adding SiO2 nanoparticles was found to be able to improve germination and seedling early
growth under salinity stress, Sabaghnia and Janmohammadi, (2014), Siddiqui and Al-Whaibi, (2014).
In similar, nano-silicon (N-Si) was shown to improve seed germination, plant growth, and
photosynthesis under environmental stresses in tomato Almutairi, (2016 a & b). Also in the case of
application of AgNPs, the alleviative effects in conditions of salt stress were found, including positive
influence on seed germination, growth of roots, and thus the overall growth and dry mass increase in
tomato seedlings under NaCl stress Almutairi, (2016a) Fig.(46),(47).
Pereira et al., (2021) reported that new agriculture revolution is needed in order to increase the
production of crops and ensure the quality and safety of food, in a sustainable way. Nanotechnology
can contribute to the sustainability of agriculture. Seed nano-priming is an efficient process that can
change seed metabolism and signaling pathways, affecting not only germination and seedling
establishment but also the entire plant lifecycle. Studies have shown various benefits of using seed
nano-priming, such as improved plant growth and development, increased productivity, and a better
nutritional quality of food. Nano-priming modulates biochemical pathways and the balance between
reactive oxygen species and plant growth hormones, resulting in the promotion of stress and diseases
resistance out coming in the reduction of pesticides and fertilizers. The present research provides
showing the challenges and possibilities concerning the use of nanotechnology in seed nano-priming,
as a contribution to sustainable agricultural practices.

339
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 46: Illustrates Seed nano-priming topics covered in this review and its potential benefits for sustainable
agriculture. In addition to providing protection for seeds during storage, the use of seed nano-priming can result
in improved establishment of plants in the soil with a reduced need for fertilizers. By growing faster, plants have
an increased ability to compete with weeds for resources, consequently increasing productivity and food quality.
The plants may also become more resistant to abiotic and biotic stresses, resulting in reduced use of pesticides.
After Pereira et al., (2021)

Fig. 47: Illustrates germination phases and reactive oxygen species (ROS) effects. (a) The germination process is
subdivided into three phases: phase I (water uptake), phase II (metabolic activity, with initiation of degradation
of starch reserves and preparation for embryo development), and phase III (embryo development and emergence

340
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

of the radicle). (b) The ROS act by destabilizing cell wall, allowing water uptake and cell elongation; (c) ROS
level in seeds and hormones production. After Pereira et al., (2021)
The combined application of AgNPs and salinity increased the soluble sugars and proline
contents. On the other hand, it decreased catalase activity and increased peroxidase activity compared
to the respective AgNP treatments alone. AgNPs enhanced the salt tolerance in wheat, but the long-
term response of AgNPs under salt stress needs further investigation. El-Sharkawy et al., (2017) have
demonstrated that application of K nanoparticles in alfalfa may be more efficient than the use of
conventional fertilizers, as the nutrition can be more adequate and this way of application may prevent
the negative effects of salt stress in some specific conditions. The abovementioned results suggest that
the application of different nanoparticles is a promising strategy to stimulate the plant tolerance to salt
stress. According to the many researchers, engineered nanoparticles have a great chance of getting into
agricultural lands Delfani et al., (2014); Benzone et al., (2015); Liu et al., (2015); Liu and Lai, (2015);
Mastronardi et al., (2015); Rastogi et al., (2017). We report that a common industrial nanoparticle could
in fact have a positive impact on crops. Modern nanofertilizers are expected to contribute to the
improvement of crop growth, photosynthesis, and tolerance to environmental stress, which will result
to better nutrient and water use efficiency and yield increase.
6.3. Effects of NPs on molecular aspects of plants
The plant’s biological functions depend on the events that occur at the molecular level. However, little
progress has been made at the molecular level influenced by NPs, which is an important step in
evaluating potential mechanisms and plants’ effects Ali et al., (2021). Certainly, NPs cannot be so
effective without interfering with cellular mechanisms and gene expression because salinity stress
affects the expression of genes and as a result influences the plant growth through changes in the
expression of many genes involved in the different parts of cells and their products Fig. (48).

Fig. 48: Illustrates the interaction of nanoparticles and soil salinity at physiological and biochemical
and molecular Levels in plants

Research in this area was performed by analyzing the expression of microRNA in NPs-treated
cells Kumar et al., (2019). According to the results of these researchers, the NPs affected the expression
of miR398 and miR408, which are responsible for regulating seed germination, the growth of roots and
seedlings, as well as antioxidants and free radical scavenger. It should also be noted that excessive
expression of microRNA causes the mentioned factors to be prevented. Therefore, it is necessary to
obtain complete information about the optimal amount of each NPs. NPs-mediated increase in root
growth is attributed to the decrease in miR164 expression, which is involved in the signaling of auxin
hormone. Increase in miR169 expression and decrease in miR167 expression can result in lateral root
production and acceleration in flowering Kumar et al., (2019); Tolaymat et al., (2017). In a study, the
simultaneous effect of Zn oxide NPs (0, 20, and 40 mg L− 1 ) and plant growth-promoting bacteria
(Bacillus subtilis, Lactobacillus casei, and Bacillus pumilus) on cytosine methylation in tomato plants

341
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

(Solanum lycopersicum L. ’Linda) was examined under 250 mM NaCl Hosseinpour et al., (2020).
While salinity stress was able to increase the polymorphism ratio, the combined use of the NPs and
bacteria reduced the DNA hyper methylation caused by salinity stress. In fact, DNA methylation is one
of the epigenetic changes in the cell for the expression of genes, and the cell changes the expression of
genes during methylation and demethylation in salinity stress Peng and Zhang, (2009). In another study,
the foliar application of Zn-NPs on rapeseed plant (Brassica napus L.) under salinity stress caused a
change in the expression of genes involved in stress to reduce the expression of some genes (e.g.,
SKRD2, MYC and MPK4) and an increase in the expression of some other genes (e.g., ARP and MPK)
associated with many physiological, hormonal and developmental responses, and MYC and SKRD2,
which are related to transcription factor and increase in abiotic stress tolerance Hezaveh et al., (2019).
In the study of Hezaveh et al. (2019), the impact of exogenously applied ZnO-NPs on rapeseed grown
under salinity stress was studied. The ZnO-NPs reduced ion leakage and improved Hill reaction thereby
affecting the stress response genes (e.g., the expression of ARP increased while that of SKRD2, MYC
and MPK4 decreased). According to these studies, the role of Zn NPs in ameliorating salinity stress is
evident; but, due to the role of Zn in the functioning of intra- and inter-cellular signaling and DNA
transcription Asha and Narain, ( 2020) and in ameliorating harsh environmental stresses such as salinity
stress Arif et al., (2020); Sofy et al., (2020), future studies should be focused on molecular effects to
deeply understand the mode of actions of the NPs under salinity stress conditions and determine the
optical concentration of Zn NPs. According to a previous study, the low doses of Zn NPs could exert
positive, while high doses caused toxicity even under non-stress conditions Molnar ´ et al., (2020).
Dubchaket et al., (2010) demonstrated that, nano-particles obtained large surface to volume rate
that promotes their bioavailability, bioactivity and biochemical activities. Bassiouny et al., (2020)
reported that, Zinc Oxide-nano or Zinc Oxide bulk raised the number of bands and density responsive
proteins in wheat cultivars (Sids 13 and Sakha 94) in absence and present of AM. The protein bands at
molecular weight 51 kDa and 40 kDa in both wheat cultivars can be considered as positive markers for
ZnO-NPs and bulk ZnO, under salinity stress and it was noted that these bands disappearing under the
control treatment. In this connection, Abedi et al., (2011), found that, in wheat plant the band with Mwt
51 kDa band might be related to Rubisco activase enzyme. Moreover, El–Bassiouny et al., (2015)
reported that protein with molecular weight of 40 kDa seems to dehydrin expressed under salinity stress
in flax cultivars. In addition, Merrick and Bruno, (2004) and Thomas et al., (2011) found that unique
gene expression patterns might help in development and validation of promising biomarkers suitable
for high-through put screening methods, and for better understanding of the toxicity of nano-particles.
Results show superiority of Sakha 94 cultivar in the number of protein bands and density responsive
proteins than Sids 13 cultivar. In this connection, Ali et al., (2007) reported that salt tolerance barley
cultivar under salt treatment were recognize by a specific band and proposed that this specific bands
might use as markers for the identification of tolerant cultivar under salt stress.
Ye et al., (2020a) investigated the effect of manganese (III) oxide NPs (0.1, 0.5 and 1 mg. L− 1
on pepper plants at 100 mM NaCl salinity level. The researchers found that the NPs penetrated through
the seed coat, forming a corona-NPs compound. A noteworthy point in this study was key role of
manganese NPs, especially at a concentration of 1 mg. L− 1 , in increased expression of superoxide
dismutase (SOD) genes, as a result production of SOD as one of the important enzymes for scavenging
ROS under salinity stress. In view of the current literature, only the afore-mentioned study reporting
the effect of Mn NPs on pepper can be detected, so molecular reports regarding Mn NPs induced
improvement in salinity stress tolerance are rare. Thus, due to role of Mn in the reinforcement of the
plant’s defense system against multiple abiotic stresses Ye et al., (2019), future research should focus
on this domain to figure out the potential and novel roles of Mn NPs in mediating salt stress tolerance.
Carbon-based NPs applications can also alleviate unfavorable environmental conditions in plants
particularly salinity stress Khan et al., (2017). Carbon nanotubes are one of the newest carbon-based
NPs that are widely used in other industries, but much research has been done on their mechanism and
effect during salinity stress Zulfiqar and Ashraf, (2021). It has been reported that multi-walled carbon
nanotubes have the ability to change genes expression involved in the antioxidant and salt overly
sensitive 1 (SOS1) system on rapeseed plant under salinity stress Zhao et al., (2019). The application
of the NPs to salt stressed rapeseed seedlings also induced intensification of nitrate reductase dependent
nitric oxide biosynthesis, re-establishment of ion and redox imbalance evidenced by the decrease in
ROS over generation, reduction in thiobarbituric acid production, and decrease in Na+/K+ ratio. The

342
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

aforementioned beneficial effects were related to the NPs induced alteration in Na+/H+ exchanger 1
(NHX1) and K+ transporter 1 (KT1) transcripts Zhao et al., (2019). Research on carbon nanomaterials
(e.g., carbon nanodots, nanofibers, nanobeads, and nano-diamonds) regarding their effects on salinity-
stressed plants is rare and hence requires future studies. Further research in this domain is certainly
required to elucidate how these carbon nanomaterials trigger some specific metabolic processes in
salinity- stressed plants. This will help to better understand the potential of carbon nanomaterials in
ameliorating salinity stress as well as to evaluate the risk related to the environment and organisms
using materials containing NPs, because high doses of multi-walled carbon nanotubes showed
phytotoxic effects as confirmed by biochemical and epifluorescence microscopy evidences Gohari et
al., (2020b). The positive effect of cerium oxide NPs also showed a significant decrease in ROS levels
and an increase in calcium content in treated plants. The NPs have been shown to affect ROS and Ca2+
mediated signaling genes. In fact, the ROS and Ca2+ are important and effective in response to stress in
plants. Cerium NPs were also able to affect terpene synthetase genes (CAD1 and TPS) An et al., (2020).
The interesting point in this study was that the NPs were found only in seed tissue and were not found
in seedling tissues and claimed that the effects of the NPs are more related to their molecular effects.
Research on cerium NPs in inducing salinity tolerance in plants is rare. Thus, future studies should be
conducted with the major aim to evaluate the mode of actions of cerium NPs on molecular mechanisms
in plants encountering the threat of climate change associated-salinity stress. In addition, the
accumulation of cerium NPs in different plant organs was observed to be a dose-dependent phenomenon
Singh et al., (2019). Therefore, the determination of the optical concentration of Zn NPs is necessary to
achieve the best yield of the plants under salinity stress. Silicon-NPs showed positive effects on
Cannabis sativa L. under salinity stress conditions and led to improved growth and molecular changes
in this plant Guerriero et al., (2021). The results of proteomics analysis in tomato plants under salinity
stress showed that silicon affected light-harvesting complexes, cytochrome b6f (Cytb6f) and ATP-
synthase complex genes Muneer et al., (2014). Kim et al., (2014) showed that silicon treatment altered
the expression of 29 genes, including genes involved in transcription factor, kinase/phosphatase,
photosynthetic genes, and genes involved in stress. In addition to these effects, this element was
involved in increasing the expression of OsNAC protein, which is effective in responding to stress
Siddiqui et al., (2020). In addition, silicon can affect the expression of genes involved in the
biosynthesis of auxin and nitric oxide Tripathi et al., (2020a). Moreover, another mechanism that helps
to alleviate the effects of salinity stress by silicon was a change in the expression of genes such as
OsZEP, OsNCED, and OsZEP, which are involved in the biosynthesis of the hormone abscisic acid
(ABA) Tripathi et al., (2020b). It has been reported that under salinity stress, by increasing the
expression of the protein OsHMA3, silicon causes more salt transfer into the vacuole and improves
plant growth, and also protects the plant against the negative effects of stress by increasing the activity
of antioxidant enzymes Siddiqui et al., (2020). In general, according to the published studies, which are
mostly on the use of silicon in improving tolerance to salinity in plants Etesami and Jeong, (2018) and
Etesami et al., (2020), silicon NPs-mediated-growth improvement and salinity stress mitigation need
further research. Scarcity of studies related to the use of silicon-NPs for ameliorating salinity stress
demands further research in this domain. Hence, future studies should focus on the molecular
mechanisms associated with increased salinity stress tolerance achieved through the supplementation
of silicon-NPs. The role of Cu, as a micronutrient, in reducing harmful impacts of salinity on plants
(e.g., by improving water relations, photosynthesis, and nutrition and upregulating the antioxidant
defense and increased levels of osmoprotectants and amino acids) has been reported Iqbal et al., (2018).
In a study, Hernandez-Hern ´ ´ andez, et al., (2018) also assayed the effect of Cu-NPs on tomato under
salt stress and reported enhanced tomato growth by promoting the expression level of SOD and
jasmonic acid (JA) genes, which resulted in alleviating ionic and oxidative stresses. The authors
suggested that the application of Cu-NPs could effectively increase salinity tolerance by activating the
antioxidant defense mechanism and by the octadecanoid pathway of jasmonates. Although the use of
Cu-NPs for alleviating salt stress in plants is still at the infancy stage, the reports available show a
considerable potential of this micronutrient in nano-forms for imparting salinity stress tolerance in
plants Zulfiqar and Ashraf, (2021). Therefore, more research at molecular levels is required to find the
mode of actions of Cu NPs to achieve improved salinity tolerance in plants. Due to multiple benefits
related to crop improvement of Ag NPs, the use of these NPs is also making their way in agriculture.
However, there are limited studies on Ag NPs as a potential solution for alleviating the negative impact

343
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

of salinity on plants Zulfiqar and Ashraf, (2021). Hence, future studies should focus on deciphering
their role in managing salinity stress tolerance at molecular level. Many researchers approve the use of
Ag-NPs with considerable caution and care, since they can release silver ion (Ag+) in the environment,
and this ion being highly toxic in nature, can be hazardous for organisms Tortella, et al., (2020).
Therefore, it is important to know how Ag-NPs influence plant growth, and up to what extent they cause
any prospective risk to the environment and health of the organisms Yan and Chen (2019). It is known
that Fe assists plants in acquiring stress tolerance Tripathi et al., (2018). Fe NPs have also great potential
to ameliorate salinity stress in plants Abdoli et al., (2020); Moradbeygi et al., (2020), but the
information on the specific metabolic pathways (at molecular level) that they regulate is not
comprehensively available in the current literature Zulfiqar and Ashraf, (2021).

7. Role of Sulfur Metabolites under Salinity stress.

The mechanisms that plants operate under saline environment is essential beginning in efforts to
reduce the adverse effects of salinity stress. The agricultural system is tightly linked with the fertilizer
input and thus the judicious application of fertilizers is expected to lead positive effects in reversing the
salinity effects. Sulfur is a macronutrient with essential roles in plant development under optimal and
stressful environment. Several compounds are synthesized from sulfur metabolism useful in reversing
the adverse effects of abiotic stress because of their free radicals scavenging property Fig. (49).

Fig. 49: Scheme representing the assimilation of sulfur (S), its involvement in the glutathione (GSH)
synthesis, and GSH-mediated control of oxidants (reactive oxygen species, ROS) generated due to
salinity in plants. GR, glutathione reductase; GSSH, oxidized glutathione; AsA, reduced ascorbate;
MDHA, monodehydroascorbate; DHAR, Dehydroascorbate reductase; MDHAR,
monodehydroascorbate reductase; APX, ascorbate peroxidase; CAT, catalase; SOD, superoxide
dismutase. O2 −, superoxide; H2O2, hydrogen peroxide. After Rasheed et al., (2020)

Sulfur-containing metabolites, amino acids (cysteine and methionine), vitamins (biotin and
thiamine), thioredoxin system, glutathione lipoic acid and glucosinolates have potential to promote or
modify physiological and molecular processes under salinity stress in plants. Thus, modulation of sulfur
metabolites production could alter physiological and molecular mechanisms to provide tolerance
against salinity.

7.1. Role of sulfur in Salinity Tolerance

Most of the S in higher plants is taken up in the form of sulfate through sulfate transporter from
soil. Sulfate can also be taken up through leaves in the form of S gases like H2S or SO2. Sulfur
assimilation pathway and synthesis of reduced S compounds are well documented. Once S is reduced
in the cell, it either remains in cytosol or transported into the plastid or stored in the vacuole for further
metabolic reactions Fig. (50).

344
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 50: Transport processes in primary sulfur assimilation. Sulfate is taken up by the root cells with
the help of SULTR1;1 (1) and SULTR1;2 (2). Once crossed the plasma membrane of epidermal and
cortical root cells, sulfate is transported through the series of sulfate transporters (SULTR) residing in
various membranes within the plant. The SUTR4;1 and SULTR4;2 are important for the efflux from
the vacuole into the cytoplasm (3). The transporter important for the sulfate influx into vacuole is still
unknown. Import of sulfate into the chloroplasts is possible due to SULTR3;1 and probably other
members of SULTR3 subfamily (4). PAPS is produced both in chloroplasts and in the cytoplasm and
can be exchanged between these compartments by PAPST/TAAC transporter (5). The known
transporter of thiols (GSH and γEC) are chloroquine-resistance transporter (CRT)-like proteins or CRLs
(6). However, an alternative transport system for thiols in the plastid membrane is expected to exist. In
a similar way, the GSH transporters to the mitochondria await still the discovery. S-adenosylmethionine
transporter 1 (SAMT1; 7) is a chloroplastidic protein involved in the exchange of SAM with S-
adenosylhomocysteine, the by-product of methylation reactions that has to be regenerated to SAM in
the cytoplasm. This is also the case for the plasmalemma-localized transporters of S-methylmethionine
(SMM) and GSH, which are important transport form of reduced sulfur and therefore need to be
exported out of the cell. APS, adenosine 5′-phosphosulfate; Cys, cysteine; OAS, O-acetylserine; γEC,
γ-glutamylcysteine; GSH, glutathione; SAM, S-adenosylmethionine; PAPS, 3′-phosphoadenosine-5′-
phosphosulfate; PAP, 3′-phosphoadenosine 5′-phosphate. Dashed lines indicate theoretically possible
transport pathways. After Gigolashvili, and Kopriva, (2014)

The assimilation of S is highly regulated in a demand-driven manner Lappartient and Touraine,

(1996). First step in S assimilation involves the activation of sulfate to adenosine 5’-phosphosulfate
(APS) catalyzed by ATP sulfurylase (ATP-S; EC 2.7.7.4). A relatively minor extension of this pathway
is the phosphorylation of APS to 3’-phosphoadenosine-5’-phosphosulfate (PAPS), catalyzed by APS
kinase (APK; EC: 2.7.1.25). Subsequently, APS is reduced to sulfite by APS reductase (APR; EC:
1.8.99.2) and the sulfite is further reduced to sulfide by a ferredoxin-dependent sulfite reductase (SiR;
EC: 1.8.7.1) and the sulfide is incorporated into the amino acid skeleton of O-acetyl-L-Serine (OAS)
by O-acetyl-L-Serine (thiol) lyase (OAS-TL), forming Cys Leustek et al., (2000). Serine acetyl
transferase (SAT; E.C 2.3.1.30), catalyzes the formation of OAS from L-Serine and acetyl-CoA links
the serine metabolism to Cys biosynthesis Takahashi et al., (2011). Subsequently, Cys is formed by the
condensation of sulfide and OAS, catalyzed by cysteine synthase (CSase) Fig. (51).

345
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 51: Illustrates sulfate assimilation pathway in plants. ATPS, ATP sulfurylase; APS, adenosine-5′-
phosphosulfate; APK, APS kinase; PAPS, 3′-phosphoadenosine-5′ phosphosulfate; APR, APS
reductase; SIR, sulfite reductase; SAT, Ser acetyltransferase; OAS, O-acetyl-Ser; OAS-TL, OAS
(thiol)lyase; γ-EC, γ-glutamyl-Cys; γ-ECS, γ-EC synthetase; GSH, red. Glutathione; GSHS, GSH
synthetase; GSSG, ox. Glutathione; Fd, ferredoxin. After Gerlich et al., (2018)

Synthesis of Cys and the activity of SAT and OAS-TL are strongly regulated by protein-protein
interactions in the multi-enzyme complex of CSase Berkowitz et al., (2002); Droux, (2003). Activity
of SAT is strongly activated by association with OAS-TL, which is inactive and has only a regulatory
role in the complex. The bound SAT exhibited higher apparent affinity for its substrate, acetyl-CoA and
L-serine that might offer the possibility of regulation of synthesis of Cys in plants Droux et al., (1998).
Consequently, the formation of Cys is the crucial step for assimilation of reduced S into S-containing
organic compounds. Plants have potential to develop several mechanisms to overcome the adverse
effects of salinity stress. Among all strategies adopted by plants to cope salinity stress, availability of S
along with S-containing compounds is of paramount importance. ATP-S is considered as the first rate-
limiting enzyme of the S assimilation pathway and is up regulated under salinity stress Ruiz and
Blumwald, (2002). It has been shown that salinity regulates key enzyme of sulfate assimilation, APR
activity; mRNA levels of three APR isoforms increased by 3-folds with 150 mM NaCl treatment.
Moreover, the increase in APR activity can be correlated with a higher rate of Cys synthesis to adjust
the increased demand for GSH Koprivova and Kopriva, (2008). The activity of other enzymes of sulfate
assimilation, SAT and salinity Ruiz and Blumwald, (2002) induce a cytosolic isoform of OAS-TL. It
has been reported that salinity induces transcription and translation of OAS-TL genes probably due to
higher demand of Cys or other S-containing compounds required by the plant as an
adaptation/protection against higher level of salinity Romero et al., (2001). Most abundant cytosolic
OAS-TL isoform, OAS-A1, is known to be involved in the defense responses of Arabidopsis against
salinity Barroso et al., (1999), Dominguez-Solís et al., (2001). The activity of OAS-TL was found
increased under salinity in Typha and Phragmites contributing substantially to satisfy the higher demand
of Cys for adaptation and protection. Higher Cys synthesis in both the plants supports the efficiency of
the thiol-metabolism based tolerance Fediuc et al., (2005). The over-expression of CSase, or SAT, key
enzymes of Cys biosynthesis was related to higher tolerance to oxidative stress and the overexpression
of these enzymes is considered promising tool for engineering S assimilation for higher Cys and GSH
synthesis Noji and Saito, (2007) Gene expression of Atcys-3A, coding for cytosolic OAS-TL, was
induced as a tolerance mechanism under salinity Barroso et al., (1999). In salt-treated plants, sufficient
Sulfur supply allows GSH synthesis necessary to prevent the adverse effects of ROS on photosynthesis.
Plants with higher levels of thiol compounds in S-sufficient plants were more able to remove the toxic
effects of salinity and were more salinity tolerant Astolfi and Zuchi, (2013). Overexpression of BrECS1
and BrECS2 in transgenic rice plants tolerated high salinity by maintaining a cellular redox state, which
prevented unnecessary membrane oxidation. These rice plants also showed lower relative ion leakage
and higher chlorophyll-fluorescence than wild type rice plants on exposure to salt, resulting in enhanced
tolerance to abiotic stresses Bae et al., (2013)

346
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

7.2. Sulfur Metabolites in Salinity Tolerance

Sulfur is a ubiquitous and essential element for all living organisms from bacteria to animals and
plants. Sulfur played many important roles in plants under optimal and stressful environments, but
cannot involve directly in any specific metabolic role in plants Fig. (52).

Fig. 52: Summary of the major outcomes. The involvement of NO/ETH with supplementation of N and
S in eviation toxicity of salt stress. APX, ascorbate peroxidase; AVG, 1-aminoethoxy vinyl glycine;
ETH, ethylene; cPTIO, 4-(carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxy-3-oxide; CAT,
catalase; Cys, cysteine; GR, glutathione reductase; GSH, reduced glutathione; GSSG, oxidized
glutathione; N, nitrogen; NO, nitric oxide; NUE, nitrogen use efficiency; S, sulfur; SOD, superoxide
dismutase; SUE, sulfur use efficiency. After Jahan et al., (2021)

Jahan et al., (2021) reported that stated that salt, stress significantly contributes to major losses
in agricultural productivity worldwide. The sustainable approach for salinity-accrued toxicity has been
explored. The use of plant growth regulators/phytohormones, mineral nutrients and other signaling
molecules is one of the major approaches for reversing salt-induced toxicity in plants. Application of
the signaling molecules such as such as nitrogen (N) and sulfur (S) play significant roles in combatting
the major consequences of salt stress impacts in plants.
Maintenance of the S-status and the major biochemical and molecular studies to this end have
reported to improve plant abiotic stress tolerance Per et al., (2016), Fatma et al., (2016). In fact, S-
containing compounds (including cysteine, Cys; glutathione, GSH) significantly help in cellular redox
homeostasis and thereby minimize plant protection against oxidative stress Fatma et al., (2014); Kumar
et al., (2018). GSH acts as an important water-soluble and low molecular weight antioxidant; a major
component of AsA-GSH cycle; and the main non-protein source of S to the plants Seth et al., (2012),
Iqbal et al., (2021). Furthermore, GSH interacts with diverse stress and defense-related signaling
molecules and can modulate their pathways, thereby combatting stress-impacts Kumar etal (2018).
Adequate S-supply can enhance the content of GSH and improve photosynthetic and growth
characteristics in salt stressed plants Fatma et al., (2021), Fatma et al., (2014). The imposition of salt
stress significantly increased S-assimilation and the biosynthesis of Cys and GSH Jahan et al., (2020).
In addition, S-supplementation was also observed to improve ascorbic acid (AsA), total phenolics,
tocopherol, lycopene, and antioxidant capacity, and decreased H2O2 and MDA content in Z. mays
under salt conditions Riffat et al., (2020). S-supply can also attenuate the inhibitory effects of salt stress
on gas exchange attributes and growth of lettuce plants, decrease Na+/K+ ratio, and improve uptake of
K and P de Souza et al., (2019). Moreover, supplementation of S reduced the electrolyte leakage and
Na+ accumulation while increasing K+ and Ca2+ and photosynthetic rate under high salt-stressed
sunflower plants Aziz et al., (2019).
They also stated that the coordinated actions between N and S have emerged as an important
strategy for improving plant growth and productivity under environmental stresses Jahan et al., (2021),

347
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Nazar et al., (2011). In fact, there occurs functional convergence and good coordination between N and
S uptake, reduction assimilatory pathways Jahan et al., (2020); Coleto et al., (2017) and Jobe et al.,
(2019). The status of nitrate reductase (NR; involved in N-assimilation) and ATP-sulfurylase (ATP-S;
involved in S-assimilation) showed mutual interaction in terms of their coordinated role in Cys-
synthesis and GSH-production Jahan et al., (2020). Particularly, there exists a close relation among
GSH and S and N Jahan et al., (2020). The availability of its constituent amino acids, Cys, glutamine
and glycine are connected with the biosynthesis of GSH which contains three moles of N per mole of
S. Notably, the glutamine synthetase (GS)-glutamate synthase (GOGAT) pathway of N assimilation
yields glutamic acid; whereas, S-assimilation ends with Cys synthesis Jahan et al., (2020). In this way,
the coordinative functions of S and N may strengthen plant capacity for stress tolerance. The literature
is full on the recognition of regulatory interactions between N and S assimilation, and its significance
in plant stress tolerance Jahan et al., (2020), Nazar et al., (2011), and Prodhan et al., (2019). The
synergistic relationship of N and S also contributed in enhancing plant growth, photosynthetic
efficiency and proline accumulation under salt stress Rais et al., (2013). The basal supplementation of
S with foliarly applied salicylic acid (SA) to salt treated plants modulated enzymes involved in N
assimilation, and GOGAT cycle Hussain et al., (2021). During N-deficiency, hydrogen sulfide (H2S)
and rhizobia synergistically regulated assimilation and remobilization of N and modulated senescence-
associated genes expression Zhang et al., (2020). However, the literature is scanty on N-S interactive
effects in minimization of salt toxicity. The synergistic relationship of N and S also contributed to
enhancement of growth and crop productivity Prodhan et al., (2019). The relationship of N and S in
terms of crop yield and quality has also been recognized in several studies Prodhan et al., (2019). It is
imperative to unveil more insights into N-S coordination, and their cumulative role in plant salt-
tolerance at physiological/biochemical and molecular levels.
The smallest diatomic gas of Nitric oxide (NO), (30.006 g mol−1), has emerged as a gaseous
signaling molecule in plants and has also been reported to exhibit its connection with a range of
phenomena from germination and senescence to photosynthesis and cellular redox balance Per et al.,
(2017); Fatma et al.; (2016); Iqbal et al., (2021); Lancaster (2015) and Fancy et al., (2017). NO, can
easily diffuse across the plant cells and contribute to signal transduction pathways by interacting with
different cellular compounds and radicals Akram et al., (2018). Even low (µM and nM) levels of NO
can confer plant tolerance to a range of stresses including metal toxicity, salt, drought, high temperatures
by mainly modulating the major components of antioxidant defense system and thereby limiting
elevated ROS-accrued oxidative stress Jahan et al., (2020); Sehar et al., (2019); Jahan et al., (2021);
Fatma et al., (2016); Per et al., (2017) Ahmad et al., (2018) andTian et al., (2015). Both exogenous
supplementation of NO-donors [e.g., sodium nitroprusside (SNP)], NO-scavengers [e.g., 2-(4-
carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO)] and enzyme inhibitors were
widely used to elucidate NO-roles in stressed plants. NO, can activate secondary messengers and/or
induce transcription of genes and thereby control diverse processes in plants Gaupels et al., (2011).
Moreover, NO can also directly modify proteins, and react with residues of Cys (S-nitrosylation),
tyrosine (nitration), or iron and zinc in metalloproteins (metal nitrosylation) Martínez-Ruiz et al.,
(2011).
The presence of Sulfur in biomolecules is responsible for their catalytic or electro-chemical
properties and thus for their involvement in specific biochemical mechanisms. In plants, S is an essential
and integral part of amino acids i.e., Cys and Met, vitamins (biotin and thiamine), antioxidant (GSH),
fatty acid (lipoic acid) and thioredoxin systems. These biomolecules have structural or redox control in
proteins, especially Sulfur -donation in iron-S cluster and vitamin biosynthesis and detoxification of
ROS and xenobiotics Leustek et al., (2000); Droux, (2003); Droux, (2004) and Hell, (2003). In addition
to these roles, Sulfur application improved photosynthetic efficiency and growth in two cultivars of
mustard under salinity Wirtz and Droux, (2005). Cys synthesis in plants represents the final step of
assimilatory sulfate reduction and the almost exclusive entry reaction of reduced S into metabolism of
plants in a demand driven manner Kopriva and Rennenberg, (2004), Kopriva, (2006).

7.3. Amino Acids

Cysteine is the metabolic precursor of essential biomolecules such as vitamins, cofactors,
antioxidants and many defense compounds. It is synthesized in plants in the cytosol, plastids and
mitochondria by the sequential action of enzymes in S assimilationFig. (53).

348
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 53: Illustrates the sulfate assimilation and metabolism pathway. Enzymes are indicated in orange
letters. Abbreviations of metabolites: APS, adenosine 5′-phosphosulfate; PAPS, 3′-phosphoadenosine
5′-phosphosulfate; R-OH, hydroxylated precursor; Ser, serine; OAS, O-acetylserine; Cys, cysteine;
OPH, O-phosphohomoserine; Thr, threonine; Cyst, cystathionine; Hcyst, homocysteine; Met,
methionine; γ-EC, γ-glutamylcysteine; GSH, glutathione; GS-X, glutathione conjugate; Glu, glutamate;
X-Cys Gly, cysteinylglycine conjugate. Abbreviations of enzymes: ATPS, ATP sufurylase; APK, APS
kinase; SOT, sulfotransferase; APR, APS reductase; SiO, sulphite oxidase; SiR, sulfite reductase; SAT,
serine acetyltransferase; OAS-TL, OAS(thiol)lyase; CGS, cystathionine γ-synthase; TS, threonine
synthase; CBL, cystathionine β-lyase; MS, methionine synthase; γ-ECS, γ-glutamylcysteine synthetase;
GSHS, glutathione synthetase; GST, glutathione-S-transferase; GGT, γ-glutamyl transferase. After Li
et al., (2020)

SAT synthesizes the intermediary product OAS, and OAS-TL combines a sulfide with an OAS
to produce Cys. Most of the Cys is formed and accumulated in the cytosol Krueger et al., (2010) by the
action of the major cytosolic OAS-TL, encoded by OAS-A1 Lopez-Martin, (2008a), Barroso et al.,
(1995). It has been demonstrated that OAS-A1 is involved in the defense responses against abiotic
stresses Barroso et al., (1999), Dominguez-Solís et al., (2001), Domínguez-Solís et al., (2004) and is
essential for maintaining the antioxidant capacity of the cytosol Lopez-Martin, (2008a), Lopez-Martin,
(2008). In knockout oas-a1 plants, intracellular Cys and GSH levels are significantly reduced, and the
GSH redox state is shifted towards its oxidized form. Moreover, oas-a1 mutant accumulates ROS in the
absence of external stress, and show spontaneous cell death lesions in the leaves. Besides, Cys in
conserved form has paramount importance in the function and signaling of enzymatic processes under
environmental stress Meyer and Hell, (2005). Studies have shown that salinity induced higher rates of
Cys synthesis with the increased expression of the cytosolic form of OASTL, and OAS-TL was related
to salt tolerance Romero et al., (2001), Barroso et al., (1999), Fediuc et al., (2005). Ruiz and Blumwald,
(2002) showed that the increase in NaCl in the growth medium led to an increase in SAT in wild type
and transgenic canola plants. The increase in SAT was limited to only 10% in transgenic plants growing
in the presence of 150 mM NaCl, whereas wild type plants showed a marked increase in SAT activity
of about 2.5 times. The salinity induced differences in SAT activity between wild type and transgenic
plants were correlated with the leaf Cys concentrations because Cys content was found 1.5 times more
in wild-type plants than transgenic plants. Cys can be converted into Met and further to S-
adenosylmethionine (SAM) through reaction with ATP by SAM synthetase. In plants with S deficiency,

349
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

the decline in chlorophyll together with decrease in SAM by many folds has been observed Nikiforova
et al., (2005). S-containing amino acid Met is an essential amino acid and executes central role in the
initiation of mRNA translation of plants. Met is also a fundamental metabolite in plant cells as it directly
or indirectly regulates a variety of cellular processes such as the precursor of SAM, which is the primary
biological methyl group donor in cell wall synthesis, secondary metabolites, and chlorophyll synthesis,
DNA replication Amir, (2010) ethylene, glycine betaine Khan et al., (2012) nicotianamine and
polyamine Sauter et al., (2013). In addition, SAM is required for other methylation reaction of
chlorophyll biosynthesis Nikiforova et al., (2005). In addition, Met has nutritional importance in crop
plants Galili et al., (2005). Sanchez-Aguayo et al., (2004) have established a relationship between the
increased levels of SAM synthetase (enzyme in SAM synthesis from Met) content and salinity tolerance
in tomato plants. Recently, Ogawa and Mitsuya, (2012) showed that utilization of S-methyl methionine
was involved in salinity tolerance at the germination and early growth stages of Arabidopsis. Thus,
plant development under stress conditions could be augmented with enhanced Met metabolism. The
derivatives of methionine, ethylene and polyamines (PAs) have also been shown to induce salinity
tolerance in plants. Cao et al., (2008) have given an insight into the link between ethylene signaling
pathway and salinity tolerance. They also showed that ethylene signaling modulates salt response at
different levels, including membrane receptors, components in cytoplasm, and nuclear transcription
factors in the pathway. Recently, Abbas and Morris, (2013) showed that MAPK signal transduction
pathways are important to salt tolerance. The over expressed transgenic barley lines had constitutively
higher levels of ethylene with jasmonic acid and showed tolerance to salinity; and after two weeks of
salt treatment barley transgenic plants showed less reduction in growth. Polyamines are Met derivative
plant growth regulators which include putrescine, cadaverine, spermidine and spermine. The tolerance
of plants induced by PAs has been correlated with elevated levels of putrescine, spermidine or spermine
Alcázar et al., (2010). In a study, Yamaguchi et al., (2006) have found that absence of spermine causes
an imbalance in calcium homeostasis in the mutant plant in high salinity responses. In several other
studies, putrescine, spermidine and spermine have shown potential in enhancing salt tolerance in plants
Roy and Wu, (2001), (2002).

7.4. Vitamins
Vitamin generally links with the necessary dietary factors for animals. However, in general, plants are
the only sources of vitamins. S is a core substance in nutritional vitamins i.e., biotin or vitamin H and
thiamine or vitamin B1 Fig. (54).

Fig. 54: Illustrates the structure of (a) thiamine hydrochloride and (b) biotin.

Biotin is a water-soluble vitamin biosynthesized by plants and is required by all living organisms
for normal cellular functions and growth Che et al., (2003). In plants, biotin plays a role as coenzyme
that binds covalently to lysine residue of a group of enzymes and catalyzes many of reactions including
carboxylation and decarboxylation Moss and Lane, (1971). Besides acting as a catalytic cofactor, biotin
has a critical role in the enzymological mechanism of a number of enzymes that are essential in both
catabolic and anabolic metabolic processes. Che et al. Che et al., (2003) demonstrated that biotin has
additional non-catalytic functions in regulating gene expression in Arabidopsis plants. Biotin controls
expression of the biotin-containing enzyme, methyl crotonyl-coenzyme A (CoA) carboxylase by
modulating the transcriptional, translational and/or post-translational regulation of this enzyme.
Similarly, Li et al., (2012) suggested that biotin deficiency resulted in spontaneous cell death and
modulated defense gene expression. However, role of biotin under salinity is not well studied until date,
but Hamdia, (2000) have studied the influence of biotin in ameliorating the effects of salinity on growth
and metabolism in lupine plants. More research is needed to evaluate the role of biotin in salinity

350
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

tolerance. Due to the abundance of thiamine in whole grains and green vegetables, plants represent the
primary dietary source of thiamine in human and animal diets. Thiamine in the form of thiamine
pyrophosphate (TPP), acts as a cofactor for several enzymes in key cellular metabolic pathways such
as glycolysis, the pentose phosphate pathway and the tricarboxylic acid cycle (TCA); and in amino acid
and isoprenoid biosynthesis Tunc-Ozdemir et al., (2009). Another form of thiamine is thiamine
diphosphate (TDP), a coenzyme in a number of metabolic reactions including acetyl-CoA synthesis,
TCA cycle, anaerobic fermentation, oxidative pentose phosphate pathway, the Calvin cycle and plant
pigment biosynthesis Friedrich, (1987), Rapala-Kozik et al., (2008). Rapala-Kozik et al., (2008)
observed responses of Zea mays seedlings to abiotic stress including salinity and suggested the
involvement of TDP-dependent enzymes metabolism under stress conditions. Total thiamine content in
maize seedling leaves increased under salinity stress and the increase was found associated with changes
in the relative distribution of free thiamine, thiamine monophosphate (TMP) and TDP suggesting a role
of thiamine metabolism in the plants’ response to salinity. In another study, Rapala-Kozik, et al., (2008)
has shown the involvement of biosynthesis of thiamine compounds and thiamine diphosphate-
dependent enzymes in salinity and osmotic stress sensing and adaptation processes in Arabidopsis
thaliana. El-Shintinawy and El-Shourbagy, (2001) observed that the addition of thiamine in 100 mM
NaCl concentration alleviated the reduction of growth in plants and further they described that
alleviation was correlated to the induction of 20 kDa and 24 kDa low molecular proteins in total protein
content and increased contents of Cys and Met.

7.5. Thioredoxin System

Thioredoxins are small (12-13 KDa), ubiquitous and heat stable proteins found in all types of
organisms. Thioredoxins are believed to regulate the cell redox with active disulfide bridge Schurmann
and Jacquot, (2000) with a conserved pair of vicinal Cys (-Trp-Cys-Gly-Pro-Cys-Lys-) Holmgren,
(1989) . There are two distinct families of thioredoxins based on sequence of amino acids. Family I:
one distinct thioredoxin domain whereas family II: fusion of proteins with one or more thioredoxin
domains with additional domains Gelhaye et al., (2004). Furthermore, family I is classified into six
major groups: the thioredoxins f, h, m, o, x and y in higher plants. Thioredoxins f, m, x and y belong to
chloroplasts, whereas the thioredoxin o is found in plant mitochondria. Marti et al., (2011) showed a
role of mitochondrial thioredoxin PsTrxo1 as a component of the defense system induced by 150 mM
salt in pea mitochondria. The increase in mitochondrial Trx activity was observed in response to NaCl
treatment was correlated to mechanism by which plants respond to salinity Fig. (55), and protects
mitochondria from oxidative stress together with antioxidant enzyme. Similarly, Fernandez
Trijueque, (2012) by using pea seedlings mRNA expression profile of the plastic PsTRX m1showed
that TRX is expressed in cotyledons. Furthermore, the response of plastid TRXs to NaCl and its
potential in restoring growth of TRX-deficient yeast under saline conditions was studied. It was
suggested that there was reserve mobilization in seedling cotyledons and physiological functions of
PsTRX m1 in the salinity response during germination. Zhang, et al., (2011) have reported that
OsTRXh1 regulates the redox state of the apoplast and influences plant development and salinity
responses.

351
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 55: Schematic model showing the main responses of TRX o1 mutant plants to salt and/or
drought/drought recovery. Two independent studies have recently demonstrated that several
physiological processes related to metabolism, stomatal function and antioxidant metabolism are
affected in Arabidopsis thaliana plants with knockout of the mitochondrial TRX o1. 27, 29. The
inactivation of TRX o1 leads to increases and decreases in both primary and secondary metabolism
during drought and recovery, respectively27 (further details are found in the main text). Moreover,
stomatal function is affected in the mutants under salinity and drought recovery: lower water loss and
higher stomatal closure under salinity but higher stomatal conductance (gs) following drought recovery
were observed. Although higher levels of H2O2 and lipid peroxidation were found in these plants, it
seems that increased activities of antioxidative enzymes such as Mn-SOD, Fe-SOD, Cu/ZnSOD, GR
and catalase are likely able to counteract TRX o1 deficiency in arabidopsis mutant plants under salinity.
After Da Fonseca-Pereira et al., (2019)

Da Fonseca-Pereira et al., (2019), Redox reactions substantially influence the activity of several
proteins and participate in the regulation of crucial cellular processes. Kocsy et al., (2013). Accordingly,
a growing body of evidence has highlighted the importance of the thioredoxins (TRXs) for the redox
control of plant metabolism. Guggenberger et al., (2017), Buchanan (2016) TRXs are small proteins
containing a redox active disulfide group within its catalytic domain. Being widely distributed
throughout most living cells, Yano, (2014). TRXs are involved in a variety of cellular redox reactions.
Numerous isoforms of TRXs are present in plants, differing in both amino acid sequence and subcellular
localization. Over 20 isoforms have been identified in the genome of Arabidopsis and grouped into
seven subfamilies (f-, m-, h-, o-, x- y-, and z-types). Belin et al., (2015), Thormählen et al., (2015). The
vast majority of TRXs isoforms are located in the chloroplast, but TRXs are also present in mitochondria
(TRXs o and h) and cytosol (TRX h), where the presence of highly similar isoforms of NADPH-
dependent TRX reductase (NTR), A and B, complete a functional TRX system. Montrichard et al.,
(2009), Reichheld et al., (2004), Non-plastid TRX system also includes proteins located at the nucleus
(TRXs h-type in wheat seeds, Serrato and Cejudo, (2003), Pulido et al., (2009) NTRA in Arabidopsis
Marchal et al., (2014) and pea Martí et al., (2009) and TRX o1 in pea leaves Calderón et al., (2017),
endoplasmic reticulum Traverso et al., (2013) (TRXs h2, h7, and h8) and attached to the plasma
membrane Meng et al., (2010) (TRX h9). The redox regulation of chloroplast function has received
considerable attention over the last decades; however, the functional role of redox processes in other
cell compartments remains unclear. For instance, the functional role of the extraplastidial NTR/TRX
system remains poorly understood, most likely due to the extensive functional redundancies between

352
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

TRXs and glutaredoxins (GRXs) and also between NTRs found in both mitochondria and cytosol. Belin
et al., (2015); Reichheld et al., (2010) The introduction of proteomics-based approaches to TRX studies
have greatly contributed to the identification of putative TRX targets in plants, especially in the
mitochondria. Montrichard et al., (2009), Balmer et al., (2004), Nietzel et al., (2017). Since then,
hundreds of putative targets involved in a broad spectrum of mitochondrial processes have been
identified, including photorespiration, tricarboxylic acid (TCA) cycle and associated reactions, ATP
synthesis, hormone synthesis, and stress-related reactions. Balmer et al., (2004), Yoshida et al., (2013).
However, it is important to emphasize that such proteomic approaches provide substantial false-positive
interactions and also lack the information whether the TRX-target interaction identified in vitro also
occurs in vivo. Thus, further experiments with mutants and/or recombinant proteins are needed to fully
elucidate the functionality of the TRX-target proteins interaction. In this vein, experimental validation
successfully demonstrated that alternative oxidase (AOX) Gelhaye et al., (2004) and some of the
enzymes of the TCA cycle including isocitrate dehydrogenase, Yoshida and Hisabori, (2014) citrate
synthase, Stevens et al., (1997), Schmidtmann et al., (2014) succinate dehydrogenase, and fumarase are
regulated by the mitochondrial TRX system in vitro and/or in vivo. Daloso et al., (2015). Furthermore,
cytosolic malate dehydrogenase has also been demonstrated to be regulated by TRXs. Hara et al.,
(2006). The mechanisms that coordinate mitochondrial TRX regulation and its implications for the
dynamic of plant metabolism under different stresses conditions are poorly understood. However, the
significance of mitochondrial redox metabolism in cellular signaling processes coupled with studies of
different loss-of-function mutants have recently enabled us to grasp the importance of mitochondrial
TRXs under stress conditions. Daloso et al., (2015), Da Fonseca-Pereira et al., (2019), Calderón et al.,
(2018). In order to gain further insights into the physiological and metabolic function of the
mitochondrial TRX/NTR system, we have recently investigated the significance of the mitochondrial
TRX system under consecutive drought episodes. Using the Arabidopsis ntra ntrb double mutant and
two independent mitochondrial trxo1 mutants, our study demonstrated that the lack of a functional
mitochondrial NTR/TRX system enhances drought tolerance following single and multiple events of
drought. Da Fonseca-Pereira et al., (2019). Extensive metabolic and physiological analyses of these
mutants revealed multiple and complex responses following both single and repetitive drought episodes.
Da Fonseca-Pereira et al., (2019) Notably, TRX o1 transcripts were more highly expressed under
drought, an effect that was even stronger during repetitive drought/recovery events. Da Fonseca-Pereira
et al., (2019) Compelling evidence from several plant species indicates that AOX transcript and protein
increase during drought (reviewed in Vanlerberghe et al., (2016)). Given that TRX o1 may function in
the reductive activation of AOX, Martí et al., (2009) further investigation to elucidate whether the
proposed protective role for TRX o1 under drought Da Fonseca-Pereira et al., (2019) and salinity Ortiz-
Espín et al., (2017), Calderón et al., (2018) is possibly also associated to the redox modulation of AOX.
Notwithstanding, we further showed that the levels of a large number of secondary metabolites
(glucosinolates, anthocyanins, flavonol glycosides, and hydroxycinnamates) increased in at least one of
the TRX mutants following two cycles of drought. Da Fonseca-Pereira et al., (2019). This result
reinforces the idea that secondary metabolism is redox-regulated by TRX system. Daloso et al., (2015),
Bashandy et al., (2009). What remains unclear and thus deserve further investigation is which enzymes
of the secondary metabolism are the target of TRXs. Additionally; our study demonstrated that TRX
mediated redox regulation seems to be crucial for stomatal function following the plant recovery from
a second drought event, Da Fonseca-Pereira et al., (2019). Similar to the situation observed under water
limitation, compensatory readjustments were also observed in the responses of plants lacking the
mitochondrial TRX o1 following salt stress. These responses included alterations in the glutathione
redox state and/or up-regulation of AOX Martí et al., (2011), and antioxidant enzymes. Ortiz-Espín et
al., (2017), Calderón et al., (2018). Fig. (56). Moreover, Attrxo1 seeds germinated faster and
accumulated higher H2O2 content under salinity, suggesting that TRX o1 could act as a sensor under
salinity and/or an inducer of H2O2 accumulation. Ortiz-Espín et al., (2017), the expression of the
antioxidant enzymes AtPRXIIF and AtSRX was not altered during germination in either water or NaCl.
Ortiz-Espín et al., (2017), conversely, in pea plants the expression of TRX o1 and PRXIIF increased in
response to shortterm salt stress Martí et al., (2011), Barranco-Medina et al., (2008) highlighting to the
heterogeneity of the antioxidant system depending on the stress condition, which may in turn be related
to specific TRX o1 targets following seed germination, a point that clearly deserves further
investigation. Ortiz-Espín et al., (2017), collectively, these observations are in good agreement with our

353
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

proposal that perturbation of mitochondrial TRX affects cellular redox metabolism in general. It seems
likely that in the absence of a functional mitochondrial TRX system the main mechanisms used to
maintain redox homeostasis under drought/salt include an increased concentration of secondary
metabolites and higher activities of enzymes of redox metabolism such as superoxide dismutase and
catalase Fig. (56). Moreover, stomatal behavior allowing higher stomatal closure during salt stress
Calderón et al., (2018), and better recovery of stomatal conductance following rehydration Da Fonseca-
Pereira et al., (2019) Fig. (56) was shown to be a key factor for the maintenance of plant growth. To
further elucidate the physiological performance of the TRX mutant lines after drought, here we
compared the relationship between the ratio of electron transport rate (ETR) and net photosynthesis
(AN) versus stomatal conductance (gs) (extracted from Da Fonseca-Pereira et al., (2019). Both
parameters can be employed as physiological status indicators. Flexas et al., (2002), Flexas et al., (2002)
ETR/AN ratio reflects the energy transfer to the photosynthesis. Under optimum conditions, AN is the
main sink, however, under stress AN is more sensitive and reduces faster than ETR, promoting the ratio
increase and indicating an energy impairment that can be associated to ROS production. Flexas et al.,
(2002) Accordingly, following drought recovery after drought (irrigation for 3 days) an inverse
relationship between both parameters was observed, where WT plants displayed higher ETR/AN
(indicating higher physiological stress) accompanied by lower gs; meanwhile TRX mutant lines showed
comparatively lower ratios with higher gs for the same recovery period Fig. (56).

Fig. 56: Relationship between the ratio of electron transport rate (ETR) and net photosynthesis (AN)
versus stomatal conductance (gs) in TRX Arabidopsis knockout mutants. The genotypes used here were
ntra ntrb, trxo1-1 and trxo1-2, and wild-type plants (WT) during dehydration and following rehydration.
Data was calculated from da Fonseca-Pereira et al. 2019.27 Regression coefficient and P value are
shown.**Means the significant difference of the relationship between AN/ETR x gs. in a two-tailed
Fisher’s exact test (P< 0.001). After Da Fonseca-Pereira et al., (2019)

In addition, Serrato et al., (2004) reported a novel NADPH thioredoxin reductase (NTR) in the
chloroplast. Deficiency of NTR caused hypersensitivity to salinity in Arabidopsis thaliana as
Arabidopsis NTRC knockout mutant showed growth inhibition and hypersensitivity to salinity and
suggested the role of NTRC gene in plant protection against oxidative stress.

7.6. Glutathione
Studies have shown the up-regulation of Cys synthesis in plants in response to salinity, suggesting
a definite possible role of thiol in salt stress tolerance. Salinity creates over production of ROS and
causes adverse effects on plant growth and metabolism that may be associated with the disturbances in
osmotic potential of soil leading to osmotic stress or specific ion toxicity Munns and Tester, (2008) Fig.
(57).

354
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Fig. 57: Schematic model summarizing the results presented in this study. Mutation in a tau group
glutathione transferase (AtGSTU) gene supposedly induced the accumulation of ROS and lipid
peroxides, which led to a temporary oxidized redox state within the cells, accompanied by elevated
Dehydroascorbate and oxidized glutathione levels. After Horváth et al., (202)

Horváth et al., (2020) reported that, high levels of reduced GSH are advantageous as they act as
a strong buffer against ROS but would make the system less responsive to changes in redox potential
that may be needed to up regulate the inducible defence components as reported by Schwarzländer et
al., (2008). Proteomic analysis of Arabidopsis roots subjected to the 150 mM NaCl treatment revealed
an increase in the amount of important ROS-scavenging and detoxifying proteins, including APX,
glutathione peroxidase, Class III peroxidases, SOD and GSTs Jiang et al., (2006). In the present study,
we found that the salt stress was accompanied by enhanced DHAR and GR activities. Knockout
Atgstu24 also had higher DHAR activity and GSH content after salt treatment than wild-type plants
and this could help to keep ROS under tight control and maintain a higher AsA/DHA and GSH/GSSG
ratio. However, taking into account that the Atgstu24 mutant had slightly lower vitality than the other
two genotypes, it can be assumed that these changes were not suitable to allow the plant to cope
successfully with salt stress. Although the lack of AtGSTU24 increased the total GST activity under
control conditions and it was slightly elevated even after salt treatment, the induction of several
AtGSTU genes (AtGSTU3-6, AtGSTU9, AtGSTU11 and AtGSTU12) observed after salt treatment
was in most cases lower than in Atgstu19 or wild-type plants. In the Atgstu19 mutant, the GSH content
was also increased, but the GSH to GSSG ratio was lower than in Col-0. Interestingly, the calculated
redox potential from the measured data revealed similar redox status in this mutant than in the wild
type, both under control conditions and two days after application of the salt stress. By analyzing the
redox status of Arabidopsis root tips using a roGFP1 redox sensor, Jiang et al., (2016) demonstrated
that the immersion of seedlings in 100 mM of NaCl for 3–24 h shifted the redox potential of the entire
root toward the more oxidized status at the beginning, but it was re-established after 6 h and more
negative redox potentials were detected compared to control roots, especially in the case of 24 h long
treatment. Generally, the redox potential of roots depended on the strength and duration of the applied
stress: while it might remain more negative in the case of mild (50 mM NaCl) stress, it became more
oxidized in the presence of a higher (150 mM) salt concentration. However, after a few days, the salt-
induced changes in redox potentials decreased and the differences in the redox status of seedlings
practically disappeared Jiang et al., (2016). Investigation of the redox status of five-day-old Atgstu19
and Atgstf8 mutants using a roGFP2 fluorescent probe revealed that the Atgstu19 mutant had the most
oxidized redox status in all root zones and under all investigated conditions Horváth et al., (2019).

355
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Interestingly, the redox potential of the mutant roots showed smaller changes after applying 150 mM
NaCl for 3 h than the wild type, due to the fact of their already more positive value under control
conditions. It was concluded that their increased salt sensitivity can be associated with the decreased
redox potential response Horváth et al., (2019). The lower GSH/GSSG ratio and increased GSH level
observed in several GST mutants and overexpressing lines Roxas et al., (2000), Kilili et al., (2004) and
references above) suggest that altering the redox homeostasis can be part of a general mode of action
in the mechanisms of GSTs. The dynamic interaction of GSTs with other glutathione-related enzymes
might be how temporary redox status changes allow the regulation of normal cellular physiology. A
schematic model illustrating predicted physiological and regulatory events in Atgstu mutants resulting
in the observed changes in metabolite concentrations and enzyme activities under control conditions
and after applying salt stress are summarized in Fig.(57) .To compensate these changes in Atgstu
mutants the ascorbic acid and glutathione biosynthesis, the enzymatic antioxidant system (such as
Dehydroascorbate reductase and glutathione reductase activity) was induced and the AtGSTU gene
expression pattern was modified. The alteration of the ROS-processing network might help to maintain
the ROS and redox homeostasis in the mutants. Salt stress presumably intensified the accumulation of
ROS, LOOH and oxidized non-enzymatic antioxidants leading to further enhancement of the AsA and
GSH biosynthesis, the activity of antioxidant enzymes (DHAR and GR) and the expression of several
AtGSTU genes. Although these changes helped Atgstu mutants to restore the redox potential after NaCl
treatment, the vitality of mutants was lower than in wild type. (An upward arrow indicates increase
while a downward arrow shows decrease; the thickness of the arrows refers to the extent of the changes).
Abbreviations: AsA, ascorbic acid; DHA, Dehydroascorbate; DHAR, Dehydroascorbate reductase;
GSH, reduced glutathione; GR, glutathione reductase; GSSG, oxidized glutathione; GSTU, glutathione
transferase tau group; LOOH, lipid peroxides; ROS, reactive oxygen species
In order to cope the salt-induced adverse effects, plants develop defense mechanisms that include
the up-regulation of synthesis of GSH that has essential roles within the plant metabolism in reducing
the adverse effects of salinity stress Nazar et al., (2011). GSH is a low-molecular weight S metabolite
(thiol), nonenzymic antioxidant found in most of the cells. Synthesis of GSH is well regulated by S in
a demand driven manner. Sulfate withdrawal from the growing medium decreases the levels of sulfate,
Cys and GSH in plants leading to the up-regulation of sulfate transport systems and key enzymes of S
assimilatory pathway Lappartient and Touraine, (1996). It has been observed that increases in GSH
synthesis are associated with up-regulation of the Cys synthesis. Similarly, S assimilation pathway
enzymes have been found to be involved in the regulation of GSH synthesis. Queval et al., (2009)
reported that GSH accumulation was triggered by stress that resulted in the up-regulation of APR and
SAT. Regulation of the GSH synthesis is dependent on the cell compartmentation as mitochondrial
SAT is able to make major contribution to Cys synthesis under optimal conditions Haas et al., (2008),
Watanabe, et al., (2008) whereas, the SAT in chloroplast was strongly induced during H2O2 triggered
accumulation of GSH Queval et al., (2009). Oxidation state of GSH homeostasis (GSH/GSSG) can
maintain cellular redox of GSH in plant cells May et al., (1998). The capacity of GSH to participate in
the redox regulation in plant cells is, largely, dependent on its absolute concentration and the ratio of
GSH/GSSG under salinity stress Nazar et al., (2011); Khan et al., (2012). The cellular GSH redox buffer
present in cells forms major basis of redox homeostasis by which thiols proteins can maintain their
redox state and can be reverted to their reduced form. Moreover, GSH is not only a redox buffer for
cell, it also acts as an electron donor for scavenging of ROS in the major metabolic pathways of plants
like photosynthesis, respiration or sulfate assimilation. Sensitivity of plants to salt plays a major role in
the GSH-mediated tolerance. Recently, Nazar et al., (2011) have shown that Vigna radiata cultivars
differing in salt tolerance have different rate of GSH biosynthesis; the GSH content was higher in salt
tolerant than salt sensitive cultivar. The salt sensitive cultivar showed greater oxidative damage than
salt tolerant cultivar. A study on Lycopersicon esculentum has also shown that salt sensitive plants
contained lesser GSH content and redox state than the salt tolerant plants Shalata et al., (2001). Similar
reports are also available in Oryza sativa Vaidyanathan et al., (2003) and Arachis hypogaea Jain et al.,
(2002). GSH biosynthesis and its turnover differed in salt tolerant Lycopersicon esculentum and its wild
relative Lycopersicon pennellii Mittova et al., (2003), and the salt tolerant plants were able to maintain
favorable GSH/GSSG redox state within 15 days in response to salt stress. Wild type Brassica napus
plants accumulated higher GSH upon salt stress suggesting its protective role against salt-induced
oxidative damage, whereas transgenic plants did not show these antioxidative responses Ruiz and

356
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Blumwald, (2002). In Nicotiana, tobacum transgenics overexpressing glyoxalase enzymes (NtglyI) and
(NtglyII) either alone or together at 200 mM NaCl maintained higher GSH levels under salt stress.
These plants showed enhanced basal activity of GSH and suffered minimal salinity stress induced
oxidative damage measured as lipid peroxidation Yadav et al., (2005) Fig. (58).

Fig. 58: Retardation of MG- and salt stress-promoted senescence in transgenic tobacco plants
overexpressing either gly I (GI), gly II (GII), or both gly I and II in double transgenics (GIII), indicating
the tolerance at cellular levels toward toxic levels of MG and salt. Phenotypic differences (A) and
chlorophyll content (B) (gg of fresh weight) from MG-treated leaf discs of WT and various transgenic
plants (GI, GII, and GIII) after incubation in 5 and 10 mM solutions of MG for 48 h are shown. Discs
floated in water served as the experimental control. Phenotypic differences (C) and chlorophyll content
(D) (g.g of fresh weight) from sodium chloride-treated leaf discs of WT and various transgenic plants
(GI, GII, and GI+II) after incubation in 400 and 800 mM solutions of NaCl for 3 and 5 days are shown.
Discs floated in water served as the experimental control. The standard deviation in each case is
represented by the vertical bar in each graph (n = 3). Note the difference in retention of chlorophyll in
WT and transgenic plants. After Singla-Pareek, (2003)

Singla-Pareek, (2003) reported that glyoxalase pathway involving glyoxalase I (gly I) and
glyoxalase II (gly II) enzymes is required for glutathione-based detoxification of methylglyoxal. We
had earlier indicated the potential of gly I as a probable candidate gene in conferring salinity tolerance.
We report here that overexpression of gly I+ II together confers improved salinity tolerance, thus
offering another effective strategy for manipulating stress tolerance in crop plants. We have
overexpressed the gly II gene either alone in untransformed plants or with gly I transgenic background.
Both types of these transgenic plants stably expressed the foreign protein, and the enzyme activity was
higher. Compared with nontransformants, several independent gly II transgenic lines showed improved
capability for tolerating exposure to high methylglyoxal and NaCl concentration and were able to grow,
flower, and set normal viable seeds under continuous salinity stress conditions. Importantly, the double
transgenic lines always showed a better response than either of the single gene-transformed lines and
WT plants under salinity stress. Ionic measurements revealed higher accumulation of Na+ and K+ in old
leaves and negligible accumulation of Na+ in seeds of transgenic lines as compared with the WT plants.
Comparison of various growth parameters and seed production demonstrated that there is hardly any
yield penalty in the double transgenics under nonstress conditions and that these plants suffered only
5% loss in total productivity when grown in 200 mM NaCl. These findings establish the potential of
manipulation of the glyoxalase pathway for increased salinity tolerance without affecting yield in crop
plants.

357
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

In contrast, Jaleel et al., (2007) reported that treatment of salinity at 80 mM concentration to

Catharanthus roseus resulted in decreased GSH content when compared with control plants. A number
of reports are available on the response of GSH to salt stress, but its mode of action in coping salt stress
needs elaborative studies. The integrated knowledge on physiological, biochemical and molecular
approaches may provide deeper insights towards the precise roles and mechanism of GSH involved in
salt stress tolerance. Lipoic Acid Lipoic acid (LA) is derived from octanoic acid, contains two S atoms
connected by a disulfide bond at C-6 and C-8 of its chemical structure and is soluble in both water and
lipid phase. Its antioxidative property and protective nature, both in reduced form as dihydrolipoic acid
(DHLA) and oxidised form as LA have been suggested Navari-Izzo et al., (1988). Bast and Haenen,
(1988) reported that DHLA can reduce GSH and can be a good tool for detoxification of ROS in a
stressful environment. However, it can also have pro-oxidant properties by its iron-reducing ability and
by its ability to generate S-containing radicals that can damage proteins Navari-Izzo et al., (2002).
Perez-Lopez et al., (2010) have shown that the presence of LA in barley leaves occurred in the reduced
as well as in oxidized forms under non-salinized and salinized conditions. They found that non-salinized
conditions represent LA that was present mainly in reduced form i.e. DHLA and was partly involved in
the tolerance of barley to elevated salinity. In the same report, the effects of salinity were mitigated and
were correlated to a higher constitutive level of LA, which was believed to improve regeneration of
DHA, and GSSG under salinity. Tarchoune et al., (2013) explained the role of LA and DHLA in salinity
tolerance in basil (Ocimum basilicum). They have shown that salt tolerance was dependent on cultivar
and salt exposure time as adaptive response was associated with higher constitutive amounts of
tocopherols with a maximum ability of roots to use DHLA to maintain growth-making basil tolerant to
salinity. Glucosinolates are a class of secondary metabolites having S as integral part of its structure
and mainly found in Brassica crops like oilseed rape, broccoli and cabbage. Although, physiological
significance of glucosinolates in plants is not clear but it is assumed that glucosinolates has a role in
plant-pathogen interaction Del et al., (2013). Besides pathogen interaction, glucosinolates metabolism
has role in tolerance of environmental factors including saline condition. Glucosinolates accumulation
in response to environmental stress has been studied showing that some environmental factors can
change the glucosinolates content and changes in the glucosinolate profile under stress is variable for
plant adaptation. López-Berenguer et al., (2008) showed the influence of salinity level for
glucosinolates content and found that salinity level at 40 mM increased total glucosinolates content
while it decreased at 80 mM concentration of salt stress suggesting that glucosinolates have potential
to versatile role under salt stress. This variation in the glucosinolates content may be related to the
developmental stage of plants Pang et al., (2012). It has been suggested that increased glucosinolates
was involved in osmotic adjustment and salt tolerance with low water potential in boroccoli plants
López-Berenguer et al., (2009). The glucoerucin (a type of glucosinolates) content in broccoli sprouts
was increased by NaCl treatment whereas total glucosinolates reduced under salt stress. Salt treatment
at 60 mmol/L for 5 d maintained higher biomass and comparatively higher content of glucosinolates in
sprouts of broccoli Guo et al., (2013). Allocation of glucosinolates could be one of the tolerance
strategies to cope with stressful conditions with relative low energy cost. Bekaert et al., (2012) has
reported a direct allocation of glucosinolates production in Arabidopsis with an increase in
photosynthetic energy. These all findings indicated that salt-induced increases in glucosinolates content
may be involved in the salt stress response of plants but the effects of salinity on glucosinolates
biosynthesis and metabolism need further attention at molecular and cellular levels.

Conclusions and Future prospects

Salinization of soils and water resources is likely to increase as global climate change continues.
These natural resources are critical to crop food production and environmental and human health and
thus further pressures and negative implications under salinization of agroecosystems are among the
very realistic scenarios for the near future, Various preventive and proactive solutions have been applied
over time in salt-stressed agroecosystems to improve plant nutrition.
- Some relatively new and modern approaches such as microbe–plant associations have been shown
to be very effective in alleviating various agricultural constraints, including salt stress. Although in
some cases, the full results are still unknown or contradictory (e.g., negative effects on some biota).
Multidisciplinary approaches and solutions driven not only by plant and agri-environmental
scientists, but also those from other areas (remote sensing, artificial intelligence, machine learning,

358
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

big data analyses), can ensure very useful tools for detecting, protecting, and controlling salinization.
A wide range of sustainable preventive and proactive (reclamation) approaches separately and/or in
combination to improve plant salt resistance and crop nutrition under salt-affected conditions. The
most applicative strategies are controlled water management over the applications of modern, low
pressurized, and localized irrigation , and if necessary, surface/underground drainage systems . Both
systems can help maintain salinized groundwater levels below the critical root zone level and leach
concentrated salts from the rhizosphere.
- Salt-affected areas often overlap with water-stressed, organically depleted, and poorly structured
sandy soils, which are knowingly compatible for implementation in land and water conservation
practices and can additionally, underpin crop nutrition under saline conditions. Organic amendments
promote the benefits of different organic amendments for plant growth particularly in saline/sodic
soils creating the reduction of oxidative and osmotic stress. The selection of a sustainable
reclamation technique and organic material is an extremely important factor for salinization
management and mitigating salt stress in plants.
- Phytohormones might be a crucial metabolic engineering target for creating salt stress-tolerant crop
plants; auxin can improve the growth performance in plants under salinity stress. Moreover,
exogenous addition of salicylic acid can effectively increase endogenous auxin and abscisic acid
content and improve the growth performance in salt-stressed , addition of jasmonic acid also seems
to have the potential to alleviate salt-induced adverse impacts in plants.
- Microbial communities present in the rhizosphere are influenced by soil chemical conditions and
plant interactions. It was confirmed that plant–micro symbiotic associations have crucial functions
in plant nutrition, plant performance, resistance to biotic stresses, and adverse environmental
conditions (nutrient imbalances, injuries by pathogens, soil acidity/alkalinity). Soil salinity (NaCl)
could suppress certain plant–microbial associations and their population activity, and organic
rhizodeposition. Metabolic profiles of the root, rhizosphere, and root exudates can be markedly
compromised in response to NaCl exposure and can differ among plant cultivars. Confirmed
antagonistic interrelations between soil salinity and microbial biomass C, resulting in a negative
impact on microbe biomass /activity. Plant–microbe interrelations, notably with particular
symbiotic-associated bacteria (e.g., N2-fixing) and/or arbuscular mycorrhizal fungi (AMF), have
been confirmed as up-and coming options for mitigating salt stress. N-fixing-associated bacteria
(AB) groups, that act as plant growth promoters improving salinity tolerance by generating specific
enzymes (e.g., 1-aminocyclopropane-1-carboxylate deaminase), metal-organic complexes (e.g.,
siderophores), and hormones, fixing atmospheric N2 and solubilizing fewer mobile phosphates to
more bioavailable forms.
- Arbuscular mycorrhizal fungi (AMF) belong to the phylum Glomeromycotan, one of the most
important groups of soil microbes that can establish symbiotic inoculation with the roots of over
80% of terrestrial plant species. Occurring microbiota of saline soils and multiple beneficial
implications for symbiotic associated glyco/halophytic species were confirmed in different study
types. AMF such as Glomus claroideum, Glomus intraradices, Glomus macrocarpum, Glomus
mosseae, Paraglomus occultum, and Rhizophagus intraradices in associated plant species with
Olive, acacia and citrus trees, corn, Sesbania aegyptiaca can mitigate salt stress. Enhancing plant
growth over improvement of water absorption capacity, nutrient acquisition and uptake,
accumulation of different osmoregulator (proline, betaines, and polyamines, antioxidants) to adjust
cell osmopotential, physiological processes and molecular performance.
- Foliar-stabilized silicic acid can be classified as a biostimulants and has been shown to be very
efficient against abiotic and biotic stresses, which deserves much more attention in the future study.
- Effect of Si on the expression of SOS and HTK genes. However, the detailed regulatory mechanisms
of Si on SOS signaling pathways and possible interaction between Si and other salt stress sensors
remain obscure. Si transporters belong to the NIP sub-family of the aquaporin family.

References
Abass, M., and P.C. Morris, 2013. The Hordeum vulgare signalling protein MAP. kinase 4 is a regulator
of biotic and abiotic stress responses. J. Plant Physiol., 170: 1353-1359.
Abbas, T., R.M. Balal, M.A. Shahid, M.A. Pervez, C.M. Ayyub, M.A. Aqueel, and M.M. Javaid, 2015.
Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus. is associated

359
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

with enhanced photosynthesis, osmoprotectants and antioxidant metabolism. Acta Physiol.

Plant, 37, 6. [CrossRef]
Abbasi, F.M., and S. Komatsu, 2004. A. proteomic approach to analyze salt responsive proteins in rice
leaf sheath. Proteomics, 4:2072–2081.
Abdallah, M.M., Z.A. Abdelgawad and H.S.M. El-Bassiouny 2016. Alleviation of the adverse effects
of salinity stress by trehalose two rice varieties. South Africa Journal of Botany, 103: 275-282.
Abd-Elbar, O.H., R.E. Farag, S.S. Eisa, and S.A. Habib, 2012. Morpho-anatomical changes in salt
stressed Kallar grass (Leptochloa fusca L. Kunth. Res. J. Agric. Biol. Sci., 8: 158–166.
Abdel-Haliem, M.E.F., H.S. Hegazy, N.S. Hassan, and D.M. Naguib, 2017. Effect of silica ions and
nano silica on rice plants under salinity stress. Ecol. Eng., 99: 282–289. [CrossRef]
Abdelly, C., A. Debez, A. Samoui, and C. Grignon, 2011. Halophyte-fodder species association may
improve nutrient availability and biomass production of the Sabkha ecosystem. In: Öztürk M.
et al., (eds) Sabkha ecosystems, tasks for vegetation science. Springer, D. ordrecht, the
Netherlands, 85–94.
Abdelly, C., Z. Barhoumi, T. Ghanya, A. Debez, K. Ben Hamed, N. Sleimi, Z. Ouerghi, A. Smaoui, B.
Huchzermeyer, and C. Grignon, 2006. Potential utilization of halophytes for the rehabilitation
and valorization of salt-affected areas in Tunisia. In: Öztürk M, Waisel Y, K.han MA, Görk G.
(eds) Biosaline agriculture and salinity tolerance in plants. Birkhäuser Verlag, Basel
Abdoli, S., K. Ghassemi-Golezani, and S. Alizadeh-Salteh, 2020. Responses of ajowan
(Trachyspermum ammi L). to exogenous salicylic acid and iron oxide nanoparticles under salt
stress. Environ. Sci. Pollut. Res. 27: 36939–36953.
Abdullah, Z., M.A. Khan, and T.J. Flowers 2001. Causes of sterility in seed set of rice under salinity
stress. J. Agron. Crop Sci., 167:25–32.
Abebe, T., A.C. Guenzi, B. Martin, and J.C. Cushman 2003. Tolerance of mannitol-accumulating
transgenic wheat to water stress and salinity. Plant Physiol., 131:1748–1755.
Abedi, T., A. Alemzadeh and S.A. Kazemeini, 2011. Wheat yield and grain protein response to nitrogen
amount and timing. Australian Journal of Crop Science, 5 (3): 330-336.
Abrah´am, E., I.P. Salam´o, C. Koncz, and L. Szabados, 2011. “Identification of Arabidopsis and
Thellungiella genes involved in salt tolerance by novel genetic system,” Acta Biologica
Szegediensis, 55(1): 53–57.
Agarie S., N. Hanaoka, O. Ueno et al., 1998. “Effects of silicon on tolerance to water deficit and heat
stress in rice plants (Oryza sativa L)., monitored by electrolyte leakage,” Plant Production
Science, 1(2): 96–103.
Agarwal S. and R. Shaheen, 2007. “Stimulation of antioxidant system and lipid peroxidation by abiotic
stresses in leaves of Momordica charantia,” Brazilian Journal of Plant Physiology, 19(2): 149–
161.
Agarwal, P.K., P.S. Shukla, K. Gupta, and B. Jha, 2013. Bioengineering for salinity tolerance in plants:
state of the art. Mol. Biotechnol., 54:102–123.
Aghaei, K., A.A. Ehsanpour, and S. Komatsu, 2008. Proteome analysis of potato under salt stress. J.
Proteome Res., 7:4858–4868.
Ahmad P. and S. Umar, 2011.Oxidative Stress: Role of Antioxidants in Plants, Studium Press, New
Delhi, India.
Ahmad, H., S. Hayat, M. Ali, H. Liu, X. Chen, J. Li, et al., 2020. The protective role of 28-
homobrassinolide and glomus versiforme in cucumber to withstand saline stress. Plants, 9:42.
doi: 10.3390/plants9010042
Ahmad, H., S. Hayat, M. Ali, T. Liu, and Z. Cheng, 2018. The combination of arbuscular mycorrhizal
fungi inoculation (Glomus versiforme. and 28-homobrassinolide spraying intervals improves
growth by enhancing photosynthesis, nutrient absorption, and antioxidant system in cucumber
(Cucumis sativus L). under salinity. Ecol. E8: 5724–5740. doi: 10.1002/ece3.4112
Ahmad, P., A.A. Arafat, H. Abeer, F.A. Elsayed, G. Salih and P.T. Lam-Son 2016. Nitric Oxide
Mitigates Salt Stress by Regulating Levels of Osmolytes and Antioxidant Enzymes in
Chickpea, F. rontiers in Plant Science | www.frontiersin.org, 7: 347.
Ahmad, P., A.M. Abass, A.M. Nasser, L. Wijaya, P. Alam, and M. Ashraf, 2018. Mitigation of sodium
chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric
oxide. J. Plant Interact., 13: 64–72. [CrossRef]

360
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Ahmad, P., and S. Sharma, 2008. Salt stress and phyto-biochemical responses of plants. Plant Soil
Environ., 54:89–99.
Ahmad, P., C.A. Jaleel, and S. Sharma, 2010b. Antioxidative defence system, lipid peroxidation,
prolinemetabolizing enzymes and biochemical activity in two genotypes of Morus alba L.
subjectedto NaCl stress. Russ. J. Plant Physiol., 57:509–517.
Ahmad, P., C.A. Jaleel, M.A. Salem, G. Nabi, and S. Sharma, 2010a. Roles of enzymatic and non-
enzymaticantioxidants in plants during abiotic stress. Crit. Rev. Biotechnol., 30:161–175.
Ahmad, P., C.A. Jeleel, M.M. Azooz, and G. Nabi, 2009. Generation of ROS. and non-enzymatic
antioxidants during abiotic stress in Plants. Bot. Res. Intern., 2:11–20.
Ahmad, P., G. Nabi, and M. Ashraf, 2011. Cadmium-induced oxidative damage in mustard [Brassica
juncea(L). Czern.& Coss.] plants can be alleviated by salicylic acid. South Afr. J. Bot., 77:36–
44
Ahmad, P., K.R. Hakeem, A. Kumar, M. Ashraf, and N.A. Akram, 2012. Salt induced changes in
photosyntheticactivity and oxidative defense system of three cultivars of mustard (Brassica
juncea L). Afr. J. Biotechnol., 11:2694–2703.
Ahmad, R., C.J. Lim, and S.-Y. Kwon, 2013. “Glycine betaine: a versatile compound with great
potential for gene pyramiding to improve crop plant performance against environmental
stresses,” Plant Biotechnology Reports, 7: 49–57.
Akbarimoghaddam, H., M. Galavi, A. Ghanbari, and N. Panjehkeh, 2011. Salinity effects on seed
germination and seedling growth of bread wheat cultivars. Trakia, J. Sci., 9:43–50.
Akram, M., S. Akhtar, I. Javed, A. Wahid, and R. Rasul, 2002. Anatomical attributes of different wheat
(Triticum aestivum. accessions/varieties to NaCl salinity. Int. J. Agric. Biol., 4, 166–168.
Akram, N.A., and M. Ashraf, 2011. Improvement in growth, chlorophyll pigments and photosynthetic
performance in salt-stressed plants of sunflower (Helianthus animus L). by foliar application of
5-aminolevulinic acid. Agrochimica Pica, 55: 94–104.
Akram, N.A., M. Iqbal, A. Muhammad, M. Ashraf, F. Al-Qurainy, and S. Shafiq, 2018. Aminolevulinic
acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica
napus L). under drought stress. Protoplasma, 255: 163–174. [CrossRef] [PubMed]
Alam, P., A. Mohammed, A.A. Abdulaziz, A.A. Maged, and A. Thamer, 2022. Silicon Nanoparticle-
Induced Regulation of Carbohydrate Metabolism, Photosynthesis, A.lam and ROS.
Homeostasis in Solanum lycopersicum Subjected to Salinity Stress, A.CS. Omega, 7:
31834−31844
Alamgir A.N.M. and M. Yousuf Ali, 1999. “Effect of salinity on leaf pigments, sugar and protein
concentrations and chloroplast ATPase activity of rice (Oryza sativa L).,” Bangladesh Journal
of Botany, 28(2): 145–149.
Alamri, S., Y. Hu, S. Mukherjee, T. Aftab, S. Fahad, and A. Raza, 2020. Silicon induced postponement
of leaf senescence is accompanied by modulation of antioxidative defense and ion homeostasis
in mustard (Brassica juncea. seedlings exposed to salinity and drought stress. Plant Physiol.
Biochem. 157: 47–59. Doi: 10.1016/j.plaphy.2020.09.038
Alc´azar, R., F. Marco, J.C. Cuevas, et al., 2006. “Involvement of polyamines in plant response to
abiotic stress,” Biotechnology Letters, 28(23): 1867–1876.
Alc´azar, R., J. C. Cuevas, J. Planas, et al., 2011. “Integration of polyamines in the cold acclimation
response,” Plant Science, 180(1):31–38.
Alc´azar, R., J. Planas, T. Saxena, et al., 2010. “Putrescine accumulation confers drought tolerance in
transgenic Arabidopsis plants overexpressing the homologous Arginine decarboxylase 2 gene,”
Plant Physiology and Biochemistry, 48(7): 547–552.
Alcázar, R., T. Altabella, F. Marco, C. Bortolotti, M. Reymond, et al., 2010. Polyamines: molecules
with regulatory functions in plant abiotic stress tolerance. Planta, 231: 1237-1249.
Aldesuquy, H., Z. Baka, and B. Mickky, 2014. Kinetin and spermine-mediated induction of salt
tolerance in wheat plants: Leaf area, photosynthesis and chloroplast ultrastructure of flag leaf
at ear emergence. Egypt. J. Basic Appl. Sci., 1: 77–87. [CrossRef]
Alet, A.I., D.H. S´anchez, J.C. Cuevas et al., 2012. “New insights into the role of spermine in
Arabidopsis thaliana under long-term salt stress,” Plant Science, 182(1): 94–100.
Alharby, H.F., E.M.R. Metwali, M.P. Fuller, and A.Y. Aldhebiani, 2016. Impact of application of zinc
oxide nanoparticles on callus induction, plant regeneration, element content and antioxidant

361
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

enzyme activity in tomato (Solanum lycopersicum MilL). under salt stress. Arch. Biol. Sci.,
68(4):723–735.
Ali, A., M. Mageed, I. Ahmed and S. Mariey, 2007. Genetic and molecular studies on barley salt
tolerance. Afr. Crop Sci. Conf. Proc., 8: 669–682.
Ali, S., A. Mehmood, and N. Khan, 2021. Uptake, translocation, and consequences of nanomaterials
on plant growth and stress adaptation. J. Nanomater, 1–17.
Allakhverdiev S. I., A. Sakamoto, Y. Nishiyama, M. Inaba, and N. Murata, 2000. “Ionic and osmotic
effects of NaCl-induced inactivation of photosystems I. and II. Synechococcus sp.,” Plant
Physiology, 123(3):1047–1056.
Allakhverdiev, S.I., A. Sakamoto, Y. Nishiyama, M. Inaba, and N. Murata, 2000. Ionic and osmotic
effects of NaCl-induced inactivation of photosystems I. and II. in Synechococcus sp. Plant
Physiol., 123:1047–1056.
Almutairi, Z.M., 2016a. Influence of silver nano-particles on the salt resistance of tomato (Solanum
lycopersicum L). during germination. Int. J. Agri. Biol., 18(2):449–457.
https://doi.org/10.17957/ IJAB/15.0114
Almutairi, Z.M., 2016b. Effect of nano-silicon application on the expression of salt tolerance genes in
germinating tomato (Solanum lycopersicum L). seedlings under salt stress. Plant Omics Journal,
9(1):106–114.
Alvarez, S., E.L. Marsh, S.G. Schroeder, and D.P. Schachtman, 2008. Metabolomic and proteomic
changes in the xylem sap of maize under drought. Plant Cell Environ., 31:325–340
Alvez, F.J.G., M. Baghour, G. Hao, O. Cagnac, M.P. Rodr´ıguez- Rosales, and K. Venema, 2012.
“Expression of LeNHX. isoforms in response to salt stress in salt sensitive and salt tolerant
tomato species,” Plant Physiology and Biochemistry, 51: 109–115.
Aly-Salama, K.H. and M.M. Al-Mutawa, 2009. “Glutathione-triggered mitigation in salt-induced
alterations in plasmalemma of onion epidermal cells,” International Journal of Agriculture and
Biology, 11(5): 639–642.
Amina, I., R. Saiema, A.M. Mudasir, W. Wasia, Z.M. Khalid, and A. Parvaiz, 2021. Ion homeostasis
for salinity tolerance in plants: a molecular approach, Physiologia Plantarum, 171: 578–594.
Scandinavian Plant Physiology Society, I.SSN. 0031-9317
Amir, R., 2010. Current understanding of the factors regulating methionine content in vegetative tissues
of higher plants. Amino Acids, 39: 917-931.
Amirjani, M.R., 2011. Effect of salinity stress on growth, sugar content, pigments and enzyme activity
of rice. Int. J. Bot., 7:73–81.
An, J., P. Hu, F. Li, H. Wu, Y. Shen, J.C. White, X. Tian, Z. Li, and J.P. Giraldo, 2020. Emerging
investigator series: molecular mechanisms of plant salinity stress tolerance improvement by
seed priming with cerium oxide nanoparticles. Environ. Sci. Nano, 7: 2214–2228.
Apel, K., and H. Hirt, 2004. Reactive oxygen species: metabolism, oxidative stress and signal
transduction. Annu. Rev. Plant Biol., 55:373–399.
Apse, M.P., G.S. Aharon, W.A. Snedden, and E. Blumwald, 1999. Salt tolerance conferred by over-
expression of a vacuolar Naþ/Hþ antiport in Arabidopsis. Science, 285:1256–1258.
Arafa, A.A., M.A. Khafagy, and M.F. El-Banna, 2009. The effect of glycinebetaine or ascorbic acid on
grain germination and leaf structure of sorghum plants grown under salinity stress. Aust. J.
Crop. Sci., 3:294–304.
Arenas-Huertero, C., B. Pérez, F. Rabanal, D. Blanco-Melo, C. De la Rosa, G. Estrada-Navarrete, F.
Sanchez, A. Covarrubias, and J. Reyes, 2009. Conserved and novel miRNAs in the legume
Phaseolus vulgaris in response to stress. Plant Mol. Biol., 70:385–401
Arfan, M., H.R. Athar, and M. Ashraf, 2007. Does exogenous application of salicylic acid through the
rooting medium modulate growth and photosynthetic capacity in two differently adapted spring
wheat cultivars under salt stress? J. Plant Physiol. 164, 685–694.
doi: 10.1016/j.jplph.2006.05.010
Arif, Y., P. Singh, H. Siddiqui, A. Bajguz, and S. Hayat, 2020. Salinity induced physiological and
biochemical changes in plants: an omic approach towards salt stress tolerance. In: Plant
Physiology and Biochemistry, 156: 64–77.
Arnon, D.I. and P.R. Stout, 1939. “The essentiality of certain elements in minute quantity for plants
with special reference to copper,” Plant Physiology, 14(2):371–375.

362
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Aroca, R., R. Porcel, and J.M. Ruiz-Lozano, 2011. Regulation of root water uptake under abiotic stress
conditions. J. Exp. Bot., 63, 43–57. [CrossRef] [PubMed]
Asada, K., 1994. Production and action of active oxygen species in photosynthetic tissue. In: Foyer CH,
M.ullineaux PM. (eds) Causes of photooxidative stress and amelioration of defense systems in
plants. CRC. Press, Boca Raton, 77–104.
Asada, K., 1999. “The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation
of excess photons,” Annual Review of Plant Biology, 50: 601–639.
Asha, A.B., and R. Narain, 2020. Chapter 15 - Nanomaterials properties. In: Narain, R. (ed.), Polymer
Science and Nanotechnology. Elsevier, 343–359.
Ashraf, M. and M.R. Foolad, 2007. “Roles of glycine betaine and proline in improving plant abiotic
stress resistance,” Environmental and Experimental Botany, 59(2): 206–216.
Ashraf, M. and P.J.C. Harris, 2004. Potential biochemical indicators of salinity tolerance in plants. Plant
Sci., 166: 3- 16.
Ashraf, M., 2009. Biotechnological approach of improving plant salt tolerance using antioxidants as
markers. Biotechnol. Adv., 27: 84-93.
Ashraf, M., and Q. Ali, 2008. Relative membrane permeability and activities of some antioxidant
enzymes as the key determinants of salt tolerance in canola (Brassica napus L). Environ. Exp.
Bot., 63: 266–273. doi: 10.1016/j.envexpbot.2007.11.008
Ashraf, M., and R. Sultana, 2000. Combination effect of NaCl salinity and nitrogen form on mineral
composition of sunflower plants. Biol. Plant. 43: 615–619. doi: 10.1023/A:1002860202032 doi:
10.1105/tpc.109.210313
Ashraf, M., N.A. Akram, R.N. Arteca, and M.R. Foolad, 2010. “The physiological, biochemical and
molecular roles of brassinosteroids and salicylic acid in plant processes and salt tolerance,”
Critical Reviews in Plant Sciences, 29(3): 162–190.
Askari, H., J. Edqvist, M. Hajheidari, M. Kafi, and G.H. Salekdeh, 2006. Effects of salinity levels
onproteome of Suaeda aegyptiaca leaves. Proteomics, 6:2542–2554.
Askari-Khorasgani, O., S. Emadi, F. Mortazaienezhad, and M. Pessarakli, 2017. Differential responses
of three chamomile genotypes to salinity stress with respect to physiological, morphological,
and phytochemical characteristics. J. Plant Nutr., 40(18):2619–2630.
Askary, M., S.M. Talebi, F. Amini, and A.D.B. Bangan, 2016. Effect of NaCl and iron oxide
nanoparticles on Mentha piperita essential oil composition. Environ. Exp. Biol., 14:27–32.
https://doi. org/10.22364/eeb.14.05
Aslani, F., S. Bagheri, N. Muhd Julkapli, A.S. Juraimi, F.S.G. Hashemi, and A. Baghdadi, 2014. Effects
of engineered nanomaterials on plants growth: an overview. Sci. World J., 641759.
Assaha D.V.M., U. Akihiro, S. Hirofumi, A. Rashid and W.Y. Mahmoud, 2017. The Role of Na+ and
K+ Transporters in Salt Stress Adaptation in Glycophytes, Frontiers in Physiology |
www.frontiersin.org, 8: 509.
Astolfi S, and S. Zuchi 2013. Adequate S. supply protects barley plants from adverse effects of salinity
stress by increasing thiol contents. Acta Physiol Plant, 35: 175-181.
Aziz, A., M. Ashraf, S. Sikandar, M. Asif, N. Akhtar, S.M. Shahzad, and B.H. Babar, 2019. Optimizing
sulfur for improving salt tolerance of sunflower Helianthus annuus L. Soil Environ., 38: 222–
233. [CrossRef]
Bae, M.J., Y.S. Kim, I.S. Kim, Y.H. Choe, E.J. Lee, Y.H. Kim, H.M. Park, and H.S. Yoon, 2013.
Transgenic rice overexpressing the Brassica juncea gamma-glutamyl cysteine synthetase gene
enhances tolerance to abiotic stress and improves grain yield under paddy field conditions. Mol
Breeding, 31: 931-945.
Baea, H., E. Herman, B. Bailey, H.J. Bae, and R. Sicher, 2005. Exogenous trehalose alters Arabidopsis
transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant
defense. Physiol. Plant, 125:114–126
Bajgu, A., 2014. “Nitric oxide: role in plants under abiotic stress,” in Physiological Mechanisms and
Adaptation Strategies in Plants Under Changing Environment, 137–159, Springer.
Balestrazzi, A., C. Massimo, M. Anca, D. Mattia, and C. Daniela, 2011. Genotoxic stress and DNA.
repair in plants: emerging functions and tools for improving crop productivity, Plant Cell Rep.,
30:287–295 DOI. 10.1007/s00299-010-0975-9

363
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Ballif, B.A., and J. Blenis, 2001. Molecular mechanisms mediating mammalian mitogen-
activatedprotein kinase (MAPK. kinase (MEK. -MAPK. cell survival signals. Cell Growth
Differ, 12:397–408
Balmer, Y., W.H. Vensel, C.K. Tanaka, W.J. Hurkman, E. Gelhaye, N. Rouhier, J.-P. Jacquot, W.
Manieri, P. Schurmann, and M. Droux, 2004. Thioredoxin links redox to the regulation of
fundamental processes of plant mitochondria. Proc Natl Acad Sci USA., 101:2642–2647.
PMID: 14983062. Doi: 10.1073/ pnas.0308583101.
Bandehagh, A., G.H. Salekdeh, M. Toorchi, A. Mohammadi, and S. Komatsu 2011. Comparative
proteomic analysis of canola leaves under salinity stress. Proteomics 11:1965–1975
Bar, Y., A. Apelbaum, U. Fi Kafka, and R. Goren 1997. Relationship between chloride and nitrate and
its effect on growth and mineral composition of avocado and citrus plants. J. Plant Nutr.,
20:715–731.
Barkla, B.J., R. Vera-Estrella, M. Hernandez-Coronado, and O. Pantoja, 2009. Quantitative proteomics
of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell, 21:4044–
4058
Barrag´an V., E.O. Leidi, Z. Andr´es, et al., 2012. “Ion exchangers NHX1 and NHX2 mediate active
potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis,”
Plant Cell, 24(3): 1127–1142,
Barranco-Medina, S., T. Krell, L. Bernier-Villamor, F. Sevilla, J.J. Lázaro, and K.J. Dietz, 2008.
Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF. and formation of an
ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J. Exp. Bot., 59:3259–
3269. PMID: 18632730. doi:10.1093/jxb/ern177.
Barroso, C., J.M. Vega, and C. Gotor, 1995. A. new member of the cytosolic O-acetylserine(thiollyase
gene family in Arabidopsis thaliana. FEBS. Lett., 363: 1-5.
Barroso, C., L.C. Romero, F.J. Cejudo, J.M. Vega, and C. Gotor, 1999. Salt-specific regulation of the
cytosolic O-acetylserine(thiollyase gene from Arabidopsis thaliana is dependent on abscisic
acid. Plant Mol. Biol., 40: 729-736.
Bashandy, T., L. Taconnat, J.P. Renou, Y. Meyer, and J.P. Reichheld, 2009. Accumulation of
flavonoids in an ntra ntrb mutant leads to tolerance to UV-C. Mol Plant; 2:249–258. PMID:
19825611. doi:10.1093/mp/ssn065.
Bast, A., and G.R. Haenen 1988. Interplay between lipoic acid and glutathione in the protection against
microsomal lipid peroxidation. Biochim. Biophys. Acta., 963: 558-561.
Battaglia, M., Y. Olvera-Carillo, A. Garciarrubio, and A.A. Covarrubias 2008. The enigmatic LEA.
proteins and other hydrophilins. Plant Physiol., 148:6–24.
Beck, M., G. Komis, A. Ziemann, D. Menzel, and J. Samaj, 2011. Mitogenactivated protein kinase 4 is
involved in the regulation ofmitotic and cytokinetic microtubule transitions in Arabidopsis
thaliana. New Phytol., 189:1069–1083.
Beck, M., G. Komis, J. Muller, D. Menzel, and J. Samaj 2010. Arabidopsis homologs of nucleus- and
phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for
microtubule organization. Plant Cell, 22:755–771.
Begara-Morales, J.C., B. S´anchez-Calvo, M. Chaki, et al., 2014. “Dual regulation of cytosolic scorbate
peroxidase (APX. by tyrosine nitration and S-nitrosylation,” Journal of Experimental Botany,
65(2):527–538.
Bekaert, M., P.P. Edger, C.M. Hudson, J.C. Pires, and G.C. Conant, 2012. Metabolic and evolutionary
costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol., 196: 596-
605.
Belin, C., T. Bashandy, J. Cela, V. Delorme-Hinoux, C. Riondet, and J.P. Reichheld, 2015. A.
comprehensive study of thiol reduction gene expression under stress conditions in Arabidopsis
thaliana. Plant Cell Environ. 38:299–314. PMID: 24428628. Doi: 10.1111/ pce.12276.
Ben Ahmed, C., B. Ben Rouina, S. Sensoy, M. Boukhriss, and F. Ben Abdullah, 2010. “Exogenous
proline effects on photosynthetic performance and antioxidant defense system of young olive
tree,” Journal of Agricultural and Food Chemistry, 58(7):4216–4222.
Ben Hamed, K., C. Magné, and C. Abdelly, 2014. From Halophyte Research to Halophytes Farming,
See discussions, stats, and author profiles for this publication.
https://www.researchgate.net/publication/274072817

364
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Ben Youssef, R., J. Nahida, B. Nadia, A. Alfonso, M. Cristina, P.A. Francisco and A. Chedly, 2021.
The Efficiency of Different Priming Agents for Improving Germination and Early Seedling
Growth of Local Tunisian Barley under Salinity Stress, Plant s, 10, 2264.
https://doi.org/10.3390/plants10112264
Benzon, H.R.L., M.R.U. Rubenecia, V.U. Ultra, and S.C. Lee 2015. Nano-fertilizer affects the growth,
development, and chemical properties of rice. IJAAR, 7(1):105–117
Berkowitz, O., M. Wirtz, A. Wolf, J. Kuhlmann, and R. Hell 2002. Use of biomolecular interaction
analysis to elucidate the regulatory mechanism of the cysteine synthase complex from
Arabidopsis thaliana. J. Biol. Chem., 277: 30629-30634.
Bhandal, I.S., and C.P. Malik, 1988. Potassium estimation, uptake, and its role in the physiology and
metabolism of flowering plants. Int. Rev. Cytol., 110:205–254.
Binzel M.L., F.D. Hess, R.A. Bressan, and P.M. Hasegawa, 1988. “Intracellular compartmentation of
ions in salt adapted tobacco cells,” Plant Physiology, 86:607–614.
Blaha, G., U. Stelzl, C.M. Spahn, R.K. Agrawal, J. Frank, and K.H. Nierhaus, 2000. Preparation of
functional ribosomal complexes and effect of buffer conditions on tRNA. positions observed
by cryoelectron microscopy. Methods Enzymol., 317:292–309
Blumwald, E., 2000. Sodium transport and salt tolerance in plants. Curr. Opin. Cell Biol., 12: 431–434.
[CrossRef]
Bohnert H.J., D.E. Nelson, and R.G. Jensen, 1995. “Adaptations to environmental stresses,” Plant Cell,
7(7):1099–1111.
Bordi, A., 2010. The influence of salt stress on seed germination, growth and yield of canola cultivars.
Not. Bot. Horti. Agrobo., 38:128–133.
Bosnic, P., D. Bosnic, J. Jasnic, and M. Nikolic, 2018. Silicon mediates sodium transport and
partitioning in maize under moderate salt stress. Environ. Exp. Bot., 155:681–687. [CrossRef]
Bouchereau A., A. Aziz, F. Larher, and J. Martin-Tanguy, 1999. “Polyamines and environmental
challenges: recent development,” Plant Science, 140(2):103–125,
Brumós, J., J.M. Colmenero-Flores, A. Conesa, P. Izquierdo, G. Sánchez, D.J. Iglesias, M.F. López-
Climent, A. Gómez-Cadenas, and M. Talón, 2009. Membrane transporters and carbon
metabolism implicated in chloride homeostasis differentiate salt stress responses in tolerant and
sensitive citrus stocks. Funct. Integr. Genomics, 9:293–309
Buchanan, B.B., 2016. The path to thioredoxin and redox regulation in chloroplasts. Annu Rev Plant
Biol., 67:1–24. PMID: 27128465. Doi: 10.1146/annurev-arplant-043015-111949.
Bugos, R.C., A.D. Hieber, and H.Y. Yamamoto, 1998. Xanthophyll cycle enzymes are members of the
lipocalin family, the first identified from plants. J. Biol. Chem., 273:15321–15324.
Bybordi, A., 2014 Influence of exogenous application of silicon and potassium on physiological
responses, yield, and yield components of salt-stressed wheat. Commun. Soil Sci. Plan., 46:
109–122. [CrossRef]
Calderón, A., A. Ortiz-Espín, R. Iglesias-Fernández, and P. Carbonero, 2017. Redox Biology
Thioredoxin (Trx o 1) interacts with proliferating cell nuclear antigen (PCNA) and its
overexpression a ff ects the growth of tobacco cell culture. Redox Biol.; 11:688–700. PMID:
28183062. doi:10.1016/j.redox.2017.01.018.
Calderón, A., A. Sánchez-Guerrero, A. Ortiz-Espín, I. Martínez-Alcal á, D. Camejo, A. Jiménez, and
F. Sevilla, 2018. Lack of mitochondrial thioredoxin o1 is compensated by antioxidant
components under salinity in Arabidopsis thaliana plants. Physiol Plant., 164:251–267. PMID:
29446456. doi:10.1111/ppl.12708.
Campo, S., P. Baldrich, J. Messeguer, E. Lalanne, M. Coca, and B.S. Segundo, 2014. Overexpression
of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing
membrane lipid peroxidation. Plant Physiol doi:10.1104/pp.113. 230268.
Cao, Y.R., S.Y. Chen, and J.S. Zhang, 2008. Ethylene signaling regulates salt stress response: An
overview. Plant Signal Behav., 3: 761-763.
Cao, Z., L. Rossi, C. Stowers, W. Zhang, L. Lombardini, and X. Ma, 2017. The impact of cerium oxide
nanoparticles on the physiology of soybean (Glycine max (L). Merr. under different soil
moisture conditions. Environ Sci. Pollut. Res. Int., 25(1):930–939. https://doi.org/10.1007/
s11356-017-0501-5

365
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Carpıcı, E.B., N. Celık, and G. Bayram, 2009. Effects of salt stress on germination of somemaize (Zea
mays L). cultivars Afr. J. Biotechnol., 8:4918– 4922
Chai Y.Y., C.D. Jiang, L. Shi, T.S. Shi, and W.B. Gu, 2010. “Effects of exogenous spermine on sweet
sorghum during germination under salinity,” Biologia Plantarum, 54(1):145–148.
Chakraborty, K., R.K. Sairam, and R.C. Bhattacharya, 2012. Differential expression of salt overly
sensitive pathway genes determines salinity stress tolerance in Brassica genotypes. Plant
Physiol. Biochem., 51:90–101
Chattopadhyay, A., P. Subba, A. Pandey, D. Bhushan, R. Kumar, A. Datta, S. Chakraborty, and N.
Chakraborty, 2011. Analysis of the grasspea proteome and identification of stress-responsive
proteins upon exposure to high salinity, low temperature, and abscisic acid treatment.
Phytochemistry, 72:1293–1307.
Cha-Um, S. and C. Kirdmanee, 2010. “Effect of glycinebetaine on proline, water use, and
photosynthetic efficiencies, and growth of rice seedlings under salt stress,” Turkish Journal of
Agriculture and Forestry, 34(6):517–527.
Chaves, M.M., J. Flexas, and C. Pinheiro, 2008. Photosynthesis under drought and salt stress:
Regulation mechanisms from whole plant to cell. Ann. Bot.-London, 103: 551–560. [CrossRef]
Chaves, M.M., J.P. Maroco, J.S. Pereira, 2003. Understanding plant responses to drought-from genes
to the whole plant. Funct. Plant Biol., 30:239–264.
Che, P., L.M. Weaver, E.S. Wurtele, and B.J. Nikolau, 2003. The role of biotin in regulating 3-
methylcrotonyl-coenzyme a carboxylase expression in Arabidopsis. Plant Physiol., 131: 1479-
1486.
Cheeseman, J.M., 1988. Mechanism of salinity tolerance in plants. Plant Physiol., 87:547–550.
Chen S., J. Li, S. Wang, A. H¨uttermann, and A. Altman, 2001. “Salt, nutrient uptake and transport, and
ABA. of Populus euphratica; a hybrid in response to increasing soil NaCl,” Trees—Structure
and Function, 15(3):186–194.
Chen, D., L. Yin, X. Deng, S. Wang, 2014. Silicon increases salt tolerance by influencing the two-phase
growth response to salinity in wheat (Triticum aestivum L). Acta Physiol. Plant., 36, 2531–
2535. [CrossRef]
Chen, M.-X., S.-C. Lung, Z.-Y. Du, and M.-L. Chye, 2014. Engineering plants to tolerate abiotic
stresses. Biocatalysis and agricultural biotechnology, 3:81–87.
Chen, S., N. Gollop, and B. Heuer, 2009. Proteomic analysis of salt-stressed tomato (Solanum
lycopersicum. seedlings: effect of genotype and exogenous application of glycine betaine. J.
Exp. Bot., 60: 2005–2019.
Chen, W., X. Yao, K. Cai, and J. Chen, 2011. Silicon alleviates drought stress of rice plants by
improving plant water status, photosynthesis and mineral nutrient absorption. Biol. Trace
Element Res. 142, 67–76
Cheng, Y., Y. Qi, Q. Zhu, X. Chen, N. Wang, X. Zhao, H. Chen, X. Cui, L. Xu, and W. Zhang, 2009.
New changes in the plasma-membrane-associated proteome of rice roots under salt stress.
Proteomics, 9:3100–3114.
Chitteti, B., and Z. Peng, 2007. Proteome and phosphoproteome differential expression under salinity
stress in rice (Oryza sativa. roots. J. Proteome Res., 6:1718–1727.
Choudhury, F.K., R.M. Rivero, E. Blumwald, and R. Mittler, 2017. Reactive oxygen species, abiotic
stress and stress combination. Plant J., 90: 856–867. [CrossRef] [PubMed]
Chutipaijit, S., S. Cha-um, and K. Sompornpailin, 2011. High contents of proline and
anthocyaninincrease protective response to salinity in Oryza sativa L. spp. indica. Aust. J. Crop
Sci., 5:1191–1198
Ciftci-Yilmaz, S., M.R. Morsy, L. Song, A. Coutu, B.A. Krizek, M.W. Lewis, D. Warren, J. Cushman,
E.L. Connolly, and R. Mittler, 2007. The EAR. motif of the Cys2/His2-typezinc finger protein
Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J. Biol. Chem.,
282:9260–9268.
Clause S.D. and J.M. Sasse, 1998. “Brassinosteroids: essential regulators of plant growth and
development,” Annual Review of Plant Biology, 49:427–451.
Colcombet, J., and H. Hirt, 2008. Arabidopsis MAPKs: a complex signalling network involved in
multiple biological processes. Biochem. J., 413: 217–226.

366
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Coleto, I., M. de la Peña, J. Rodríguez-Escalante, I. Bejarano, G. Glauser, P.M. Aparicio-Tejo, and D.

Marino, 2017. Leaves play a central role in the adaptation of nitrogen and sulfur metabolism to
ammonium nutrition in oilseed rape Brassica napus. BMC. Plant Biol., 17: 1–13. [CrossRef]
[PubMed]
Colmenero-Flores, J.M., D.F.-N. Juan, C.-F. Paloma, P.-T. Procopio and A.R. Miguel, 2019. Chloride
as a Beneficial Macronutrient in Higher Plants: New Roles and Regulation, I.nt. J. Mol. Sci.,
20, 4686; doi: 10.3390/ijms20194686
Cona A., G. Rea, R. Angelini, R. Federico, and P. Tavladoraki, 2006. “Functions of amine oxidases in
plant development and defence,” Trends in Plant Science, 11(2):80–88.
Conde, C., P. Silva, A. Agasse, R. Lemoine, S. Delrot, R. Tavares, and H. Geròs, 2007. Utilization and
transport of mannitol in Olea europaea and implications for salt stress tolerance. Plant Cell
Physiol., 48:42–53
Cooke, J., and M.R. Leishman, 2011. Is plant ecology more siliceous than we realize Trends Plant Sci.
16: 61–68.
Coskun, D., D.T. Britto, Y. Jean, L.M. Schulze, A. Becker, and H.J. Kronzucker, 2012. Silver ions
disrupt K+ homeostasis and cellular integrity in intact barley (Hordeum vulgare L). roots. J.
Exp. Bot., 63: 151–162. [CrossRef] [PubMed]
Coskun, D., R. Deshmukh, H. Sonah, J.G. Menzies, O. Reynolds, J.F. Ma, H.J. Kronzucker, and R.R.
Belanger, 2019. The controversies of silicon’s role in plant biology. New Phytol., 221:67–85.
[CrossRef]
Coucha, M., S.L. Elshaer, W.S. Eldahshaw, B.A. Mysona, and A.B. El-Remessy, 2015. Molecular
mechanisms of diabetic retinopathy: Potential therapeutic targets. Middle East Afr J.
Ophthalmol., 22(2):135–144. https://doi.org/10.4103/0974-9233. 154386
Crawford N.M., 2006. “Mechanisms for nitric oxide synthesis in plants,” Journal of Experimental
Botany, 57(3):471– 478.
Da Fonseca-Pereira, P., D.M. Daloso, J. Gago, F.M.D.O. Silva, J.A. CondoriApfata, I. Florez-Sarasa,
T. Tohge, J.-P. Reichheld, A. Nunes-Nesi, A.R. Fernie, and W.L. Araújo, 2019. The
mitochondrial thioredoxin system contributes to the metabolic responses under drought
episodes in arabidopsis. Plant Cell Physiol., 60:213–229. PMID: 30329109. 10.
doi:10.1093/pcp/pcy194.
Da Fonseca-Pereira, P., M.D. Danilo, G. Jorge, N.-N. Adriano and L.A. Wagner, 2019. On the role of
the plant mitochondrial thioredoxin system during abiotic stress, PLANT. SIGNALING. &
BEHAVIOR. 2019, 14(6, e1592536 (5 pages. https://doi.org/10.1080/15592324.2019.1592536
Daloso, D.M., K. Müller, T. Obata, A. Florian, T. Tohge, A. Bottcher, C. Riondet, L. Bariat, F. Carrari,
A. Nunes-Nesi, 2015. Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant
mitochondria. Proc. Natl. Acad. Sci., U.SA., 112:E1392–400. PMID: 25646482.
doi:10.1073/pnas.1424840112.
Dang, Y.P., R.C. Dalal, D.G. Mayer, M. McDonald, R. Routely, G.D. Schwenke, S.R. Buck, I.G.
Daniells, D.K. Singh, W. Manning, and N. Ferguson, 2008. High subsoil chloride
concentrations reduce soil water extraction and crop yield on Vertisols in north-eastern
Australia. Aust. J. Agric. Res., 59:321–330.
Dang, Y.P., R.C. Dalal, R. Routley, G.D. Schwenke, and I. Daniells, 2006. Subsoil constraints to grain
production in the cropping soils of the northeastern region of Australia: an overview. Aust. J.
Exp. Agric., 46:19–35.
Dani, V., W.J. Simon, M. Duranti, and R.R.D. Croy, 2005. Changes in the tobacco leaf apoplast
proteome in response to salt stress. Proteomics, 5:737– 745
Dantas, B.F., R.L. De Sa, and C.A. Aragao, 2007. Germination, initial growth and cotyledon protein
content of bean cultivars under salinity stress. Rev Bras de Sementes, 29:106–110
Das, P., I. Manna, A.K. Biswas, and M. Bandyopadhyay, 2018. Exogenous silicon alters ascorbate-
glutathione cycle in two salt-stressed indica rice cultivars (MTU. 1010 and Nonabokra.
Environ. Sci. Pollut. Res., 25: 26625–26642. [CrossRef]
Dassanayake, M., D.H. Oh, J.S. Haas, A. Hernandez, H. Hong, S. Ali, D.J. Yun, R.A. Bressan, J.K.
Zhu, H.J. Bohnert, and J.M. Cheeseman, 2011. The genome of the extremophile crucifer
Thellungiella parvula. Nat. Genet., 43:913–918.

367
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Dawood, M.G., M.T. Abdelhamid, and U. Schmidhalter, 2014. Potassium fertiliser enhances the salt-
tolerance of common bean (Phaseolus vulgaris L). J. Hortic. Sci. Biotechnol., 89: 185–192.
[CrossRef]
De Lourdes Oliveira Otoch, M., A.C. Menezes Sobreira, M.E. Farias De Arag˜ao, E.G. Orellano, M.
Da Guia Silva Lima, and D. FernandesDeMelo, 2001. “Saltmodulation of vacuolarH+-ATPase
and H+-Pyrophosphatase activities in Vigna unguiculata,” Journal of Plant Physiology,
158(5):545–551.
De Paola, D., F. Cattonaro, D. Pignone, and G. Sonnante, 2012. ThemiRNAome of globe artichoke:
conserved and novel micro RNAs and target analysis. BMC. Genomics, 13:41.
De Souza Freitas, W.E., A.B. de Oliveira, R.O. Mesquita, H.H. de Carvalho, J.T. Prisco, and E. Gomes-
Filho, 2019. Sulfur-induced salinity tolerance in lettuce is due to a better P. and K. uptake.,
lower Na/K. ratio and an efficient antioxidative defense system. Sci. Hortic. 257: 108764.
[CrossRef]
Debona, D., F.A. Rodrigues, and L.E. Datno_, 2017. Silicon’s role in abiotic and biotic plant stresses.
Annu. Rev. Phytopathol., 55: 85–107. [CrossRef]
Debona, D., F.A. Rodrigues, and L.E. Datnoff, 2017. Silicon’s role in abiotic and biotic plant stresses.
Annu. Rev. Phytopathol., 55: 85–107
Deivanai, S., R. Xavier, V. Vinod, K. Timalata, and O.F. Lim, 2011. “Role of exogenous proline in
ameliorating salt stress at early stage in two rice cultivars,” Journal of Stress Physiology &
Biochemistry, 7:157–174.
Del Carmen, M.-B.M., D.A. Moreno, and M. Carvajal 2013. The physiological importance of
glucosinolates on plant response to abiotic stress in brassica. Int. J. Mol. Sci., 14: 11607-11625.
Delfani, M., M.B. Firouzabadi, N. Farrokhi, and H. Makarian, 2014.Some physiological responses of
black-eyed pea to iron and magnesium nanofertilizers. Commun Soil Sci., Plant Anal., 45:530–
540.
Delledonne M., Y. Xia, R. A. Dixon, and C. Lamb, 1998. “Nitric oxide functions as a signal in plant
disease resistance,” Nature, 394(6693):585–588.
Demetriou, G., C. Neonaki, E. Navakoudis, and K. Kotzabasis, 2007. Salt stress impact on the molecular
structure and function of the photosynthetic apparatus—the protective role of polyamines.
Biochim Biophys Acta-Bioenerget, 1767:272–280.
Desingh, R., and G. Kanagaraj, 2007. Influence of salinity stress on photosynthesis and antioxidative
systems in two cotton varieties. Applied Plant Physiology, 33 (3– 4): 221–234.
Dietz, K.J., N. Tavakoli, C. Kluge et al., 2001. “Significance of the Vtype ATPase for the adaptation to
stressful growth conditions and its regulation on the molecular and biochemical level,” Journal
of Experimental Botany, 52(363):1969–1980.
Ding, D., L. Zhang, H. Wang, Z. Liu, Z. Zhang, and Y. Zheng, 2009. Differential expression of miRNAs
in response to salt stress in maize roots. Ann. Bot., 103:29–38.
Dionisio-Sese, M.L., and S. Tobita 1998. Antioxidant responses of rice seedlings to salinity stress. Plant
Sci., 135:1–9.
Djamei, A., A. Pitzschke, H. Nakagami, I. Rajh, and H. Hirt, 2007. Trojan horse strategy in
Agrobacterium transformation: abusing MAPK. defense signaling. Science, 318:453–456
Dolan, L., and J. Davies, 2004. Cell expansion in roots. Curr. Opin. Plant Biol., 7: 33–39. [CrossRef]
Dolatabadian, A. and R.S. Jouneghani, 2009. Impact of Exogenous Ascorbic Acid on Antioxidant
Activity and Some Physiological Traits of Common Bean Subjected to Salinity Stress, N.ot.
Bot. Hort. Agrobot. Cluj., 37 (2): 165-172.
Dolatabadian, A., and R.J. Saleh Jouneghani, 2009. Impact of exogenous ascorbic acid on antioxidant
activity and some physiological traits of common been subjected to salinity stress. Notulae
Botanicae Horti Agrobotanici Cluj-Napoca, 37 (2): 165–172.
Dolatabadian, A., S.A.M. Modarressanavy, and F. Ghanati, 2011. Effect of salinity on growth, xylem
structure and anatomical characteristics of soybean. Not. Sci. Biol., 3:41–45.
Dombrowski, J.E., J.C. Baldwin, and R.C. Martina, 2008. Cloning and characterization of a salt stress
inducible small GTPase gene from the model grass species Lolium temulentum. J. Plant
Physiol., 165:651– 661.

368
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Dominguez-Solís, J.R., G. Gutierrez-Alcalá, J.M. Vega, L.C. Romero, and C. Gotor, 2001. The
cytosolic O-acetylserine (thiollyase gene is regulated by heavy metals and can function in
cadmium tolerance. J. Biol. Chem., 276: 9297-9302.
Domínguez-Solís, J.R., M.C. López-Martín, F.J. Ager, M.D. Ynsa, L.C. Romero, et al., 2004. Increased
cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis
thaliana. Plant Biotechnol. J., 2: 469-476.
Dooki, A.D., F.J. Mayer-Posner, H. Askari, A.A. Zaiee, and G.H. Salekdeh, 2006. Proteomic responses
of rice young panicles to salinity. Proteomics, 6: 6498–6507.
Droux, M., 2003. Plant serine acetyltransferase: new insights for regulation of sulphur metabolism in
plant cells. Plant Physiol. Biochem., 41: 619-627.
Droux, M., 2004. Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynth
Res 79: 331-348.
Droux, M., M.L. Ruffet, R. Douce, and D. Job, 1998. Interactions between serine acetyltransferase and
O-acetylserine (thiol) lyase in higher plants--structural and kinetic properties of the free and
bound enzymes. Eur. J. Biochem., 255: 235-245.
Duan J., J. Li, S. Guo, and Y. Kang, 2008. “Exogenous spermidine affects polyamine metabolism in
salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance,” Journal of
Plant Physiology, 165(15):1620–1635,
Dubchak, S., A. Ogar, J.W. Mietelski and K. Turnau, 2010. “Influence of silver and titanium
nanoparticles on arbuscular mycorrhiza colonization and accumulation of radiocaesium in
Helianthus annuus,” Span. J. Agric. Res., 8: s103–S108.
Eckardt, N.A., 2009. A. new chlorophyll degradation pathway. Plant Cell, 21:700.
El Sebai, T.N., M.M.S. Abdallah, H.M.S. El-Bassiouny, and F.M. Ibrahim 2016. Amelioration of The
Adverse Effects of Salinity Stress by Using Compost, N.igella Sativa Extract or Ascorbic Acid
in Quinoa Plants. International Journal of Pharm Tech Research. 9, (6): 127-144.
El-Bassiouny H.M.S., M.M.S. Abdallah, M.A.M. El-Enany, and M.Sh. Sadak, 2020. Nano-Zinc Oxide
and Arbuscular mycorrhiza effects on physiological and biochemical aspects of wheat cultivars
under saline conditions. Pakistan journal of biological sciences, 23 (4): 478-490.
El-Bassiouny, H.M.S. and M.Sh.S. Sadak, 2015. Impact of foliar application of ascorbic acid and α-
tocopherol on antioxidant activity and some biochemical aspects of flax cultivars under salinity
stress Acta Biologica Colombiana, 20(2):209-222
El-Mashad H. and I. A.A.A. Mohamed, 2012. “Brassinolide alleviates salt stress and increases
antioxidant activity of cowpea plants (Vigna sinensis)” Protoplasma, 249(3):625–635.
El-Sharkawy, M.S., T.R. El-Beshsbeshy, E.K. Mahmoud, N.I. Abdelkader, R.M. Al-Shal, and A.M.
Missaoui, 2017. Response of alfalfa under salt stress to the application of potassium sulfate
nanoparticles. Am. J. Plant Sci., 8:1751–1773. https://doi.org/10.4236/ajps.2017.88120
El-Shintinawy, F., and M.N. El-Shourbagy, 2001. “Alleviation of changes in protein metabolism in
NaCl-stressed wheat seedlings by thiamine,” Biologia Plantarum, 44(4):541–545,
El-Shintinawy, F., and M.N. El-Shourbagy, 2001. Alleviation of changes in protein metabolism in NaCl
stressed wheat seed by thiamine. Biol. Plant, 44: 541-545.
Elstner, E.F., 1987. Metabolism of activated oxygen species. In: Davies DD. (ed.) The biochemistry of
plants, vol II, B.iochemistry of metabolism. Academic, S.an Diego, 252–315
El-Tayeb, M.A., 2005. “Response of barley grains to the interactive effect of salinity and salicylic acid,”
PlantGrowth Regulation, 45(3):215–224.
Etesami, H., and B.R. Jeong, 2018. Silicon (Si): review and future prospects on the action mechanisms
in alleviating biotic and abiotic stresses in plants. Ecotoxicol. Environ. Saf., 147: 881–896.
Etesami, H., B.R. Jeong, and M. Rizwan, 2020. The use of silicon in stressed agriculture management:
action mechanisms and future prospects. Metalloids in Plants: Advances and Future Prospects,
381–431.
Etesami, H., F. Hamideh, and R. Muhammad, 2021. Interactions of nanoparticles and salinity stress at
physiological, biochemical and molecular levels in plants: A Review, E.cotoxicology and
Environmental Safety 225 2021. 112769
Fancy, N.N., A.K. Bahlmann, and G.J. Loake, 2017. Nitric oxide functions in plant abiotic stress. Plant
Cell Environ., 40: 462–472. [CrossRef] [PubMed]

369
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

FAO, 2009. High Level Expert Forum—How to Feed the World in 2050, E.conomic and Social
Development, F.ood and Agricultural Organization of the United Nations, R.ome, I.taly.
Farooq, M., M. Hussain, A. Wakeel, and K.H.M. Siddique, 2015. Salt stress in maize: Effects, resistance
mechanisms, and management. A Review. Agron. Sustain. Dev., 35: 461–481. [CrossRef]
Fatehi, F., A. Hosseinzadeh, H. Alizadeh, T. Brimavandi, and P.C. Struik, 2012. The proteome response
of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Mol. Biol. Rep.,
39:6387–6397.
Fathi, A., M. Zahedi, and S. Torabian, 2017. Effect of interaction between salinity and nanoparticles
(Fe2O3 and ZnO) on physiological parameters of Zea mays L. J. Plant Nutr., 40 (19):2745–
2755. https://doi.org/10.1080/00103624.2013.863911
Fatma, M., A. Masood, T.S. Per, and N.A. Khan, 2016. Nitric oxide alleviates salt stress inhibited
photosynthetic performance by interacting with sulfur assimilation in mustard. Front. Plant Sci.,
7, 521. [CrossRef]
Fatma, M., A. Masood, T.S. Per, F. Rasheed, and N.A. Khan, 2016. Interplay between nitric oxide and
sulfur assimilation in salt tolerance in plants. Crop J., 4: 153–161. [CrossRef]
Fatma, M., M. Asgher, A. Masood, and N.A. Khan, 2014.Excess sulfur supplementation improves
photosynthesis and growth in mustard under salt stress through increased production of
glutathione. Environ. Exp. Bot., 107: 55–63. [CrossRef]
Fatma, M., N. Iqbal, H. Gautam, Z. Sehar, A. Sofo, I. D’Ippolito, and N.A. Khan, 2021. Ethylene and
sulfur coordinately modulate the antioxidant system and ABA. accumulation in mustard plants
under salt stress. Plants, 10, 180. [CrossRef]
Fatma, M., N. Iqbal, H. Gautam, Z. Sehar, A. Sofo, I. D’Ippolito, and N.A. Khan, 2021. Ethylene and
sulfur coordinately modulate the antioxidant system and ABA. accumulation in mustard plants
under salt stress. Plants, 10, 180. [CrossRef]
Fatma, M., N. Iqbal, Z. Sehar, M.N. Alyemeni, P. Kaushik, N.A. Khan, and P. Ahmad, 2021. Methyl
jasmonate protects the ps ii system by maintaining the stability of chloroplast d1 protein and
accelerating enzymatic antioxidants in heat-stressed wheat plants. Antioxidants, 10, 1216.
[CrossRef] [PubMed]
Fediuc, E., S.H. Lips, and L. Erdei, 2005. O-acetylserine (thiol) lyase activity in Phragmites and Typha
plants under cadmium and NaCl stress conditions and the involvement of ABA. in the stress
response. J. Plant Physiol., 162: 865-872.
Fernández-Torquemada, Y., and J.L. Sánchez-Lizaso, 2013. Effects of salinity on seed germination and
early seedling growth of the Mediterranean seagrass Posidonia oceanica (L). Delile. Estuarine,
C.oastal Shelf Sci., 119:64–70
Fernández-Trijueque, J., D. Barajas-López Jde, A. Chueca, R. Cazalis, M. Sahrawy, et al., 2012. Plastid
thioredoxins f and m are related to the developing and salinity response of post-germinating
seeds of Pisum sativum. Plant Sci., 188- 189: 82-8.
Flam-Shepherd, R., W.Q. Huynh, D. Coskun, A.M. Hamam, D.T. Britto, and H.J. Kronzucker, 2018.
Membrane fluxes, bypass flows, and sodium stress in rice: The influence of silicon. J. Exp.
Bot., 69: 1679–1692. [CrossRef]
Fleck, A.T., S. Schulze, M. Hinrichs, A. Specht, F. Waßmann, L. Schreiber, and M.K. Schenk, 2015.
Silicon promotes exodermal Casparian band formation in Si-accumulating and Si-excluding
species by forming phenol complexes. PLoS. ONE, 10, e0138555. [CrossRef]
Fleck, A.T., T. Nye, C. Repenning, F. Stahl, M. Zahn, and M.K. Schenk, 2011. Silicon enhances
suberization and lignification in roots of rice (Oryza sativa) J. Exp. Bot., 62, 2001–2011.
[CrossRef] [PubMed]
Flexas, J., and H. Medrano, 2002. Drought-inhibition of photosynthesis in C3 Plants: stomatal and non-
stomatal limitations Revisited. Ann Bot., 89:183–189. PMID: 12099349.
doi:10.1093/aob/mcf027.
Flexas, J., J. Bota, J.M. Escalona, and B.M.H. Sampol, 2002. Effects of drought on photosynthesis in
grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Funct
Plant Biol., 29: 461–471.
Flowers, T.J., 2004. “Improving crop salt tolerance,” Journal of Experimental Botany, 55(396):307–
319.

370
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Flowers, T.J., M.A. Hajibagheri, and A.R. Yeo, 1991. Ion accumulation in the cell walls of rice plants
growing under saline conditions: evidence for the Oertli hypothesis. Plant, C.ell and Environ
14:319–325.
Flowers, T.J., M.A. Hajibagheri, and N.J.W. Clipson, 1986. Halophytes. Quart. Rev. Biol., 61:313–337
Fluhr, R. and A.K. Mattoo, 1996. “Ethylene-biosynthesis and perception,” Critical Reviews in Plant
Sciences, 15:479–523,
Ford, C.W., 1984. “Accumulation of low molecular weight solutes in water-stressed tropical legumes,”
Phytochemistry, 23(5):1007–1015.
Foster, S.S.D. * and P.J. Chilton, 2003. Groundwater: the processes and global significance of aquifer
degradation. Phil. Trans. R. Soc. Lond. B. 2003. 358,–1972 1957, 2003 The Royal Society DOI.
10.1098/rstb.2003.1380, Downloaded from rstb.royalsocietypublishing.org on July 13, 2011.
Foyer, C.H., H. Lopez-Delgado, J.F. Dat, and I.M. Scott, 1997. “Hydrogen peroxide- and glutathione-
associated mechanisms of acclimatory stress tolerance and signalling,” Physiologia Plantarum,
100(2):241–254.
Fragnire, C., M. Serrano, E. Abou-Mansour, J.-P. M´etraux, and F. L’Haridon, 2011. “Salicylic acid
and its location in response to biotic and abiotic stress,” FEBS. Letters, 585(12):1847–1852,
Franco-Navarro, J.D., J. Brumos, M.A. Rosales, P. Cubero-Font, M. Talon, and J.M. Colmenero-Flores,
2016. Chloride regulates leaf cell size and water relations in tobacco plants. J. Exp. Bot., 67:
873–891. [CrossRef] [PubMed]
Franco-Navarro, J.D., M.A. Rosales, R. Álvarez, P. Cubero-Font, P. Calvo, A. Díaz-Espejo, and J.M.
Colmenero-Flores, 2019. Chloride as macronutrient increases water use efficiency by
anatomically-driven reduced stomatal conductance and increased mesophyll diffusion to CO2
. Plant J., 99: 815–831.
Friedrich, W., 1987. Thiamin (Vitamin B1, aneurin) In: Handbuchder vitamine. (ed.) Urban,
S.chwartzenberg, M.unich, 240-258.
Fukuda A. and Y. Tanaka, 2006. “Effects of ABA, auxin, and gibberellin on the expression of genes
for vacuolar H+- inorganic pyrophosphatase,H+-ATPase subunitA, andNa+/H+ antiporter in
barley,” Plant Physiology and Biochemistry, 44(5-6):351–358.
Gabbay, K.H. 1973. The sorbitol pathway and the complications of diabetes. N. Engl J. Med. 288
(16):831–836.
Gabbay, K.H. 1975. Hyperglycemia, polyol metabolism and complications of diabetes mellitus. Ann
Rev Med., 26:521–536.
Gadallah, M.A.A. 1999. Effects of proline and glycine betaine on Vicia faba response to salt stress. Biol
Plant 42:249–257
Gain, P., M.A. Mannan, P.S. Pal, M.M. Hossain, and S. Parvin, 2004. Effect of salinity on some yield
attributes of rice. Pak J. Biol. Sci., 7:760–762.
Galili, G., R. Amir, R. Hoefgen, and H. Hesse 2005. Improving the levels of essential amino acids and
sulfur metabolites in plants. Biol. Chem., 386: 817-831.
Galston, A.W., R. Kaur-Sawhney, T. Altabella, and A.F.Tiburcio, 1997. “Plant polyamines in
reproductive activity and response to abiotic stress,” Botanica Acta, 110(3):197–207.
Gao, M., R. Tao, K. Miura, A.M. Dandekar, and A. Sugiura, 2001. Transformation of Japanese
persimmon (Diospyros kaki Thunb. with apple cDNA. encoding NADP-dependent sorbitol-6-
phosphate dehydrogenase. Plant Sci., 160:837–845
Gao, X., C. Zou, L. Wang, and F. Zhang, 2005. Silicon improves water use e_ciency in maize plants. J.
Plant Nutr., 27, 1457–1470. [CrossRef]
Gao, Z., M. Sagi, and S.H. Lips, 1998. “Carbohydrate metabolism in leaves and assimilate partitioning
in fruits of tomato (Lycopersicon esculentumL). as affected by salinity,” Plant Science,
135(2):149–159.
Garcia-Olmedo, F., A. Molina, A. Segura, and M. Moreno, 1995. The defensive role of nonspecific
lipid-transfer proteins in plants. Trends. Microbiol., 3:72–74
Garg, A.K., J.K. Kim, T.G. Owens, A.P. Ranwala, Y.D. Choi, L.V. Kochian, and R.J. Wu, 2002.
Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses.
Proc. Natl. Acad. Sci. U. S. A., 99:15898–15903.
Garg, N., and G. Manchanda, 2008. Salinity and its effects on the functional biology of legumes. Acta
Physiol Plant, 30:595–618.

371
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Garg, N., and P. Bhandari, 2016. Interactive effects of silicon and arbuscular mycorrhiza in modulating
ascorbate-glutathione cycle and antioxidant scavenging capacity in differentially salt-tolerant
Cicer arietinum L. genotypes subjected to long-term salinity. Protoplasma, 253, 1325–1345.
[CrossRef]
Garg, N., and P. Bhandari, 2016. Silicon nutrition and mycorrhizal inoculations improve growth,
nutrient status, K.+/Na+ ratio and yield of Cicer arietinum L. genotypes under salinity stress.
Plant Growth Regul., 78, 371–387. [CrossRef]
Gaupels, F., G.T. Kuruthukulangarakoola, and J. Durner, 2011. Upstream and downstream signals of
nitric oxide in pathogen defence. Curr. Opin. Plant Biol., 14, 707–714. [CrossRef]
Geilfus C.M., 2018a. Chloride (CL) From nutrient to toxicant. Plant and Cell Physiology, 59, 877–886
Geissler N, S. Hussin, H.W. Koyro, 2010. Elevated atmospheric CO2 concentration enhances salinity
tolerance in Aster tripolium L. Planta, 231:583–594
Gelhaye E, N. Rouhier, J. Gérard, Y. Jolivet, J. Gualberto, et al., 2004. A. specific form of thioredoxin
h occurs in plant mitochondria and regulates the alternative oxidase. Proc. Natl. Acad. Sci. U.
S. A. 101: 14545-14550.
Gelhaye, E., N. Rouhier, J. Gérard, Y. Jolivet, J. Gualberto, N. Navrot, P.-I. Ohlsson, G. Wingsle, M.
Hirasawa, and D.B. Knaff, 2004. A. specific form of thioredoxin h occurs in plant mitochondria
and regulates the alternative oxidase. Proc. Natl. Acad. Sci., USA., 101:14545–14550. PMID:
15385674. Doi: 10.1073/ pnas.0405282101.
Gerlich, S.C., J.W. Berkley, K. Stephan, and K. Stanislav, 2018. Sulfate Metabolism in C4 Flaveria
Species Is Controlled by the Root and Connected to Serine Biosynthesis, Plant Physiology,
178:565–582, www.plantphysiol.org American Society of Plant Biologists. All Rights
Reserved.
Ghanem, A.E., E. Mohamed, A.M. Kasem, and A.A. El-Ghamery, 2021. Differential salt tolerance
strategies in three halophytes from the same ecological habitat: Augmentation of antioxidant
enzymes and compounds. Plants, 10, 1100. [CrossRef]
Ghassemi, F., A.J. Jakeman, and H.A. Nix, 1995. Salinisation of land and water resources: Human
causes, extent, management and case studies. UNSW. Press, S.ydney, A.ustralia, and CAB.
International, Wallingford, U.K. Godoy JA, L.unar S, T.orres-Schumann J, M.oreono J,
R.odrigo RM, P.intor-Toro JA. 1994. Expression, tissue distribution and subcellular
Gigolashvili, T. and K. Stanislav, 2014. Transporters in plant sulfur metabolism, F.rontiers in Plant
Science, F.rontiers website link: www.frontiersin.org
Gill, S.S., M. Tajrishi, M. Madan, and N. Tuteja, 2013. “A. DESDbox helicase functions in salinity
stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa
L. cv. PB1.,” Plant Molecular Biology, 82(1-2):1–22.
Gilroy, S., M. Bialasek, N. Suzuki, M. Gorecka, A. Devireddy, S. Karpinski, and R. Mittler, 2016. ROS,
calcium and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol.
171: 1606–1615.
Gohari, G., F. Safai, S. Panahirad, A. Akbari, F. Rasouli, M.R. Dadpour, and V. Fotopoulos, 2020b.
Modified multiwall carbon nanotubes display either phytotoxic or growth promoting and stress
protecting activity in Ocimum basilicum L. in a concentration-dependent manner.
Chemosphere, 249: 126171.
Gomathi, R., and P. Rakkiyapan, 2011. Comparative lipid peroxidation, leaf membrane thermostability,
and antioxidant system in four sugarcane genotypes differing in salt tolerance. Int. J. Plant
Physiol. Biochem. 3: 67–74.
Gomes-Filho, E., C.RF. Machado Lima, J.H. Costa, A.C. da Silva, M. daGuia Silva Lima, C.F. de
Lacerda, and J.T. Prisco 2008. Cowpea ribonuclease: properties and effect of NaCl-salinity on
its activation during seed germination and seedling establishment. Plant Cell. Rep., 27:147–
157.
Gong, H.J., D.P. Randall, and T.J. Flowers, 2006 Silicon deposition in the root reduces sodium uptake
in rice (Oryza sativa L). Seedlings by reducing bypass flow. Plant. Cell Environ. 29: 1970–
1979. [CrossRef]
Gorbe, E., and A. Calatayud, 2012. Applications of chlorophyll fluorescence imaging technique in
horticultural research: A Review. Sci. Hortic.-Amsterdam, 138:24–35. [CrossRef]

372
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Gou, T., X. Chen, R. Han, J. Liu, Y. Zhu, and H. Gong, 2020. Silicon can improve seed germination
and ameliorate oxidative damage of bud seedlings in cucumber under salt stress. Acta Physiol.
Plant. 42: 1–11
Grattan, S.R., and C.M. Grieve, 1999. Salinity-mineral nutrient relations in horticultural crops. Sci
Hortic 78:127–157.
Greenway, H., and R. Munns, 1980. Mechanisms of salt tolerance in nonhalophytes. Annu. Rev. Plant
Physiol., 31:149–190
Grime, J.P., 1977. Evidence for the existence of three primary strategies in plants and its relevance to
ecological and evolutionary theory. Am. Nat., 111:1169–1194.
Gro, F., J. Durner, and F. Gaupels, 2013. “Nitric oxide, antioxidants and prooxidants in plant defence
responses,” Frontiers in Plant Science, 4, article 419.
Gu, M.F., N. Li, X.H. Long, M. Brestic, H.B. Shao, J. Li, and S. Mbarki, 2016. Accumulation capacity
of ions in cabbage (Brassica oleracea L). Supplied with sea water. Plant Soil Environment
62(7):314–320. https://doi.org/10.17221/771/2015-PSE
Guan, B., J. Yu, X. Chen, W. Xie, and Z. Lu, 2011. Effects of salt stress and nitrogen application on
growthand ion accumulation of Suaeda salsa plants. Intl Conf Remote Sens Environ Transport
Engin, 24– 26 June, 8268–8272.
Guerriero, G., F.M. Sutera, N. Torabi-Pour, J. Renaut, J.-F. Hausman, R. Berni, H.C. Pennington, M.
Welsh, A. Dehsorkhi, and L.R. Zancan, 2021. Phyto-courier, a silicon particle-based nano-
biostimulant: evidence from cannabis sativa exposed to salinity. ACS. Nano 15, 3061–3069.
Guerriero, G., J. Hausman, and S. Legay, 2016 Silicon and the plant extracellular matrix. Front. Plant
Sci., 7, 463. [CrossRef]
Gueta-Dahan, Y., Z. Yaniv, B.A. Zilinskas, and G. Ben-Hayyim, 1997. Salt and oxidative stress:
similarand specific responses and their relation to salt tolerance in citrus. Planta, 204:460–469.
Guggenberger, P., I. Thormählen, D.M. Daloso, and A.R. Fernie, 2017. The unprecedented versatility
of the plant thioredoxin system. Trends Plant Sci., 22:249–262. PMID: 28139457.doi:10.1016/
j.tplants.2016.12.008.
Gunes, A., A. Inal, E.G. Bagci and D.J. Pilbeam. 2007. Silicon mediated changes of some physiological
and enzymatic parameters symptomatic for oxidative stress in spinach and tomato grown in
sodic- B. toxic soil. Plant Soil, 290: 103- 114.
Guo, R.F., G.F. Yuan, and Q.M. Wang 2013. Effect of NaCl treatments on glucosinolate metabolism
in broccoli sprouts. J. Zhejiang Univ. Sci. B., 14: 124-131.
Guo, Y., Q.-S. Qiu, F.J. Quintero et al., 2004. “Transgenic Evaluation of Activated Mutant Alleles of
SOS2 Reveals a Critical Requirement for Its Kinase Activity and C-Terminal Regulatory
Domain for Salt Tolerance in Arabidopsis thaliana,” Plant Cell, 16(2):435–449,
Gupta, B., and B.R. Huang, 2014 Mechanism of salinity tolerance in plants: Physiological, biochemical,
and molecular characterization. Int. J. Genom., 6: 727–740. [CrossRef] [PubMed]
Gupta, K. J., M. Stoimenova, and W.M. Kaiser, 2005. “In higher plants, only root mitochondria, but
not leaf mitochondria reduce nitrite to NO, in vitro and in situ,” Journal of Experimental Botany,
56(420):2601–2609.
Gupta, K., A. Dey, and B. Gupta, 2013. “Plant polyamines in abiotic stress responses,” Acta
Physiologiae Plantarum, 35(7):2015–2036
Gupta, K., A. Dey, and B. Gupta, 2013. “Polyamines and their role in plant osmotic stress tolerance,”
in Climate Change and Plant Abiotic Stress Tolerance, N. Tuteja and S. S. Gill, (Eds.)1053–
1072, Wiley-VCH,Weinheim, G.ermany.
Gurmani, A.R., A. Bano, S.U. Khan, J. Din, and J.L. Zhang, 2011. “Alleviation of salt stress by seed
treatment with abscisic acid (ABA) 6-benzylaminopurine (BA) and chlormequat chloride
(CCC) optimizes ion and organic matter accumulation and increases yield of rice (Oryza sativa
L).,” Australian Journal of Crop Science, 5(10):1278–1285.
Gururani, M.A., J. Venkatesh, and L.S.P. Tran, 2015. Regulation of photosynthesis during abiotic
stress-induced photoinhibition. Mol. Plant, 8:1304–1320. doi: 10.1016/j.molp.2015.05.005
Haas, F.H., C. Heeg, R. Queiroz, A. Bauer, M. Wirtz, et al., 2008. Mitochondrial serine
acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol.,
148: 1055-1067.

373
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Halfter, U., M. Ishitani, and J.K. Zhu, 2000. The Arabidopsis SOS2 protein kinase physically interacts
with and is activated by the calciumbinding protein SOS3. Proc Natl. Acad. Sci., U. S. A.
97:3735–3740.
Halliwell, B., and J.MC. Gutteridge, 1985. Free radicals in biology and medicine. Clarendon, Oxford
Halliwell, B., and J.MC. Gutteridge, 1989. Free radicals in biology and medicine, 2nd edn. Clarendon,
Oxford. halophyte and cryophyte Arabidopsis relative model system and its applicability to
molecular genetic analyses of growth and development of extremophiles. Plant Physiol
135:1718–1737.
Hamdia, M.A., 2000. Physiological studies on the influence of biotin or pyridoxine in amelioration the
effect of salinity in lupine plants. Bull. Fac. Sci. Assiut Univ., 29: 283-291.
Hameed, M., M. Ashraf, and N. Naz, 2009. Anatomical adaptations to salinity in cogon grass [Imperata
cylindrica (L). Raeuschel] from the salt range, P.akinstan. Plant Soil, 322: 229–238. [CrossRef]
Hanfrey, C., S. Sommer, M.J. Mayer, D. Burtin, and A.J. Michael, 2001. “Arabidopsis polyamine
biosynthesis: absence of ornithine decarboxylase and the mechanism of arginine decarboxylase
activity,” Plant Journal, 27(6):551–560.
Hanson, A.D., B. Rathinasabapathi, J. Rivoal, M. Burnet, M.O. Dillon, and D.A. Gage, 1994.
“Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic
engineering of stress tolerance,” Proceedings of the National Academy of Sciences of the
United States of America, 91(1):306–310.
Hanzawa, Y., A. Imai, A.J. Michael, Y. Komeda, and T. Takahashi, 2002. “Characterization of the
spermidine synthase-related gene family in Arabidopsis thaliana,” FEBS. Letters, 527(1–
3):176–180.
Hara, S., K. Motohashi, F. Arisaka, P.GN. Romano, N. Hosoya-Matsuda, N. Kikuchi, N. Fusada, and
T. Hisabori, 2006. Thioredoxin-h1 reduces and reactivates the oxidized cytosolic malate
dehydrogenase dimer in higher plants. J. Biol Chem., 281:32065–32071. PMID: 16945919.
doi:10.1074/jbc.M605784200.
Hasanuzzaman, M., and M. Fujita 2011b. Exogenous silicon treatment alleviates salinity-induced
damage in Brassica napus L. seedlings by upregulating the antioxidant defense and
methylglyoxal detoxification system. Abstract of Plant Biology 2011, A.merican Society of
Plant Biology. http://abstracts.aspb.org/pb2011/public/P10/P10001.html.
Hasanuzzaman, M., and M. Fujita, 2011a. Selenium pretreatment upregulates the antioxidant defense
and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in
rapeseed seedlings. Biol. Trace Elem. Res., 143:1758–1776.
Hasanuzzaman, M., K. Nahar, and M. Fujita, 2014. “Regulatory role of polyamines in growth,
development and abiotic stress tolerance in plants,” in Plant Adaptation to Environmental
Change: Significance of Amino Acids and Their Derivatives, 157–193.
Hasanuzzaman, M., M. Fujita, M.N. Islam, K.U. Ahamed, and K. Nahar, 2009. Performance of four
irrigatedrice varieties under different levels of salinity stress. Int. J. Integr. Biol., 6:85–90.
Hasanuzzaman, M., M.H.M. Bhuyan, K. Parvin, T.F. Bhuiyan, T.I. Anee, K. Nahar, M. Hossen, F.
Zulfiqar, M. Alam, and M. Fujita, 2021. Regulation of ROS. metabolism in plants under
environmental stress: A Review of recent experimental evidence. Int. J. Mol. Sci., 21: 8695.
[CrossRef]
Hasanuzzaman, M., M.H.M.B. Bhuyan, F. Zulfiqar, A. Raza, S.M. Mohsin, J.A. Mahmud, M. Fujita,
and V. Fotopoulos, 2020. Reactive oxygen species and antioxidant defense in plants under
abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants 9, 681.
[CrossRef] [PubMed]
Hasanuzzaman, M., M.H.R. Rakib, C.M. Abdul Awal, R. Khussboo, N. Farzana, R. Mira, N. Kamrun
and F. Masayuki, 2021. Regulation of Reactive Oxygen Species and Antioxidant Defense in
Plants under Salinity, I.nt. J. Mol. Sci. 2021, 22, 9326. https://doi.org/10.3390/ijms22179326
Hasanuzzaman, M., N. Kamrun, and F. Masayuki, 2013. Chapter 2 Plant Response to Salt Stress and
Role of Exogenous Protectants to Mitigate Salt-Induced Damages in Ecophysiology and
Responses of Plants under Salt Stress Parvaiz Ahmad M.M. Azooz M.N.V. Prasad Editors
ISBN. 978-1-4614-4746-7 ISBN. 978-1-4614-4747-4 (eBook) DOI. 10.1007/978-1-4614-
4747-4 Springer New York Heidelberg Dordrecht London.

374
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Hasegawa, P.M., 2013. “Sodium (Na+) homeostasis and salt tolerance of plants,” Environmental and
Experimental Botany, 92:19–31.
Hasegawa, P.M., R.A. Bressan, J.-K. Zhu, and H.J. Bohnert, 2000. “Plant cellular andmolecular
responses to high salinity,” Annual Review of Plant Biology, 51:463–499,
Hashimoto, T., K. Tamaki, K.-I. Suzuki, and Y. Yamada, 1998. “Molecular cloning of plant spermidine
synthases,” Plant and Cell Physiology, 39(1):73–79,
Hattori, T., S. Inanaga, E. Tanimoto, A. Lux, M. Luxová, and Y. Sugimoto, 2003. Silicon-induced
changes in viscoelastic properties of sorghum root cell walls. Plant Cell Physiol., 44: 743–749.
[CrossRef] [PubMed].
He, T. and G.R. Cramer, 1996. “Abscisic acid concentrations are correlated with leaf area reductions in
two salt-stressed rapidcycling Brassica species,” Plant and Soil, 179(1): 25–33.
Hell, R., 2003. Metabolic regulation of cysteine synthesis, sulfur assimilation. The plant sulfate
transporter family: Specialized functions, integration with whole plant nutrition. In: Sulfur
transport, assimilation in plants: Regulation interaction, signaling. (ed.) Davidian J-C, G.rill D,
D.e Kok LJ, S.tulen I, H.awkesford MJ, S.chnug E, Rennenberg H. Backhuys Publishers,
Leiden, 21-31.
Hern´andez-Hern´andez, H., A. Ju´arez-Maldonado, A. Benavides-Mendoza, H. Ortega- Ortiz, G.
Cadenas-Pliego, D. S´anchez-Aspeytia, and S. Gonz´alez-Morales, 2018. Chitosan-PVA. and
copper nanoparticles improve growth and overexpress the SOD. and JA. genes in tomato plants
under salt stress. Agronomy 8, 175.
Hezaveh, T.A., L. Pourakbar, F. Rahmani, and H. Alipour, 2019. Interactive effects of salinity and ZnO.
nanoparticles on physiological and molecular parameters of rapeseed (Brassica napus L).
Commun. Soil Sci. Plant Anal. 50: 698–715.
Holmgren, A., 1989. Thioredoxin and glutaredoxin systems. J. Biol Chem., 264: 13963-13966.
Hong, Z., K. Lakkineni, Z. Zhang, D.PS. Verma 2000. Removal of feedback inhibition of 1 pyrroline-
5-carboxylase synthetase (P5CS) results in increased proline accumulation and protection of
plants from osmotic stress. Plant Physiol., 122:1129–1136.
Hoque, M.A., M.N.A. Banu, E. Okuma et al., 2007. “Exogenous proline and glycinebetaine increase
NaCl-induced ascorbateglutathione cycle enzyme activities, and proline improves salt tolerance
more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells,” Journal of
Plant Physiology, 164(11):1457–1468.
Hoque, M.A., M.N.A. Banu, Y. Nakamura, Y. Shimoishi, and Y. Murata, 2008. “Proline and
glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and
reduce NaCl-induced damage in cultured tobacco cells,” Journal of Plant Physiology,
165(8):813–824.
Horváth, E., B. Krisztina, G. Ágnes, R. Riyazuddin, C. Gábor, and C. Dorottya and C. Jolán, 2020.
Compensation of Mutation in Arabidopsis glutathione transferase (AtGSTU) Genes under
Control or Salt Stress Conditions, I.nt. J. Mol. Sci., 21, 2349; doi:10.3390/ijms21072349
www.mdpi.com/journal/ijms.
Horváth, E., K. Bela, B. Holinka, R. Riyazuddin, Á. Gallé, Á. Hajnal, Á. Hurton, A. Fehér, and J.
Csiszár, 2019. The Arabidopsis glutathione transferases, A.tGSTF8 and AtGSTU19 are
involved in the maintenance of root redox homeostasis affecting meristem size and salt stress
sensitivity. Plant Sci., 283: 366–374. [CrossRef]
Hosseinpour, A., K. Haliloglu, K. Tolga Cinisli, G. Ozkan, H.I. Ozturk, A. Pour- Aboughadareh, and
P. Poczai, 2020. Application of zinc oxide nanoparticles and plant growth promoting bacteria
reduces genetic impairment under salt stress in tomato (Solanum lycopersicum L. ‘Linda’.
Agriculture, 10, 521.
Hu, Y., and U. Schmidhalter 2005. Drought and salinity: a comparison of their effects onmineral
nutrition of plants. J. Plant Nutr Soil Sci., 168:541–549.
Hundertmark, M., and D.K. Hincha 2008. LEA. (late embryogenesis abundant. proteins and their
encoding genes in Arabidopsis thaliana. BMC. Genomics, 9:118–139.
Hussain, K., K. Nawaz, A. Majeed et al., 2011. “Role of exogenous salicylic acid applications for salt
tolerance in violet (Viola Odorata L).,” Sarhad Journal of Agriculture, 27:171–175.

375
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Hussain, S., Z. Bai, J. Huang, X. Cao, L. Zhu, C. Zhu, J. Zhang, 2019. 1-Methylcyclopropene modulates
physiological, biochemical, and antioxidant responses of rice to different salt stress levels.
Front. Plant Sci., 10, 124. [CrossRef] [PubMed]
Hussain, S.J., N.A. Khan, N.A. Anjum, A. Masood, and M.I.R. Khan, 2021. Mechanistic elucidation of
salicylic acid and sulphur-induced defence systems, nitrogen metabolism, photosynthetic, and
growth potential of mungbean (Vigna radiata. under salt stress. J. Plant Growth Regul., 40,
1000–1016. [CrossRef]
Hussin S, N. Geissler, and H.W. Koyro, 2013. Effect of NaCl salinity on Atriplex nummularia (L). with
special emphasis on carbon and nitrogen metabolism. Acta Physiol Plant, 35:1025–1038.
Ibrar, M., M. Jabeen, J. Tabassum, F. Hussain, and I. Ilahi 2003. Salt tolerance potential of Brassica
juncea Linn. J. Sci. Tech. Univ. Peshawar, 27:79– 84.
Inan G, Q. Zhang, P. Li, Z. Wang, Z. Cao, H. Zhang, C. Zhang, T.M. Quist, S.M. Goodwin, J. Zhu, H.
Shi, B. Damsz, T. Charbaji, Q. Gong, S. Ma, M. Fredricksen, D.W. Galbraith, M.A. Jenks, D.
Rhodes, P.M. Hasegawa, H.J. Bohnert, R.J. Joly, R.A. Bressan, and J.K. Zhu, 2004. Salt cress.
An immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell, 19:2213–2224.
Iqbal, M.N., R. Rasheed, M.Y. Ashraf, M.A. Ashraf, and I. Hussain, 2018. Exogenously applied zinc
and copper mitigate salinity effect in maize (Zea mays L). by improving key physiological and
biochemical attributes. Environ. Sci. Pollut. Res. 25: 23883–23896.
Iqbal, N., S. Umar, N.A. Khan, and F.J. Corpas, 2021. Nitric oxide and hydrogen sulfide coordinately
reduce glucose sensitivity and decrease oxidative stress via ascorbate-glutathione cycle in heat-
stressed wheat (Triticum aestivum L). Plants Antioxidants, 10, 108. [CrossRef]
Isa, M., S. Bai, T. Yokoyama, J.F. Ma, Y. Ishibashi, T. Yuasa, and M. Iwaya-Inoue, 2010. Silicon
enhances growth independent of silica deposition in a low-silica rice mutant, lsi1. Plant Soil,
331, 361–375. [CrossRef]
Ishitani M., J. Liu, U. Halfter, C.-S. Kim, W. Shi, and J.- K. Zhu, 2000. “SOS3 function in plant salt
tolerance requires Nmyristoylation and calcium binding,” Plant Cell, 12(9):1667–1677.
Ivanov, A., and M. Velitchkova, 2014. “Chapter 27: Mechanisms of stimulation of photosystem I.
activity in chloroplast membranes under heat stress. Correlation between P700 Photooxidation
and Thermostability of Thylakoid Membrane Organization,” in Contemporary Problems of
Photosynthesis, 2, eds S. I. Allakhverdiev, A. B. Rubin and V. A. Shuvalov (Moscow–Izhevsk:
Izhevsk Institute of Computer Science., 377–395.
Iyengar, E.R.R., and M.P. Reddy, 1996. Photosynthesis in highly salt-tolerant plants. In: Pessaraki M.
(ed.) Handbook of photosynthesis. Marcel Dekker, New York, 897–909.
Jacoby, R.P., A.H. Millar, and N.L. Taylor, 2010. Wheat mitochondrial proteomes provide new links
between antioxidant defense and plant salinity tolerance. J. Proteome Res., 9:6595–6604.
Jahan, B., M.F. Al Ajmi, M.T. Rehman, and N.A. Khan, 2020. Treatment of nitric oxide supplemented
with nitrogen and sulfur regulates photosynthetic performance and stomatal behavior in
mustard under salt stress. Physiol. Plant, 168: 490–510. [PubMed]
Jahan, B., M.F. Al Ajmi, M.T. Rehman, and N.A. Khan, 2020. Treatment of nitric oxide supplemented
with nitrogen and sulfur regulates photosynthetic performance and stomatal behavior in
mustard under salt stress. Physiol. Plant, 168: 490–510. [PubMed].
Jahan, B., N. Iqbal, M. Fatma, Z. Sehar, A. Masood, A. Sofo, I. D’Ippolito, and N.A. Khan, 2021.
Ethylene supplementation combined with split application of nitrogen and sulfur protects salt-
inhibited photosynthesis through optimization of proline metabolism and antioxidant system in
mustard (Brassica juncea L). Plants, 10, 1303. [CrossRef] .
Jahan, B., N. Iqbal, M. Fatma, Z. Sehar, A. Masood, A. Sofo, I. D’Ippolito, and N.A. Khan, 2021.
Ethylene supplementation combined with split application of nitrogen and sulfur protects salt-
inhibited photosynthesis through optimization of proline metabolism and antioxidant system in
mustard (Brassica juncea L). Plants, 10, 1303. [CrossRef].
Jahan, B., R. Faisal, S. Zebus, F. Mehar, I. Noushina, M. Asim, A.A. Naser and A.Kh. Nafees, 2021.
Coordinated Role of Nitric Oxide, E.thylene, N.itrogen, and Sulfur in Plant Salt Stress
Tolerance, Stresses, 1: 181–199. https://doi.org/10.3390/stresses1030014
https://www.mdpi.com/journal/stresses.

376
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Jain, M., D. Choudhary, R.K. Kale, and N. Bhalla-Sarin, 2002. Salt- and glyphosateinduced increase in
glyoxalase I. activity in cell lines of groundnut (Arachis hypogaea) Physiol Plant, 114: 499-
505.
Jaleel, C.A., P. Manivannan, G.M. Lakshmanan, R. Sridharan, and R. Panneerselvam, 2007. NaCl as a
physiological modulator of proline metabolism and antioxidant potential in Phyllanthus amarus.
C.R. Biol., 330: 806-813.
James, R.A., C. Blake, C.S. Byrt, and R. Munns, 2011. “Major genes for Na+ exclusion, N.ax1 and
Nax2 (wheatHKT1;4 and HKT1;5., decrease Na+ accumulation in bread wheat leaves under
saline and waterlogged conditions,” Journal of Experimental Botany, 62(8):2939–2947.
Janowitz, T., H. Kneifel, and M. Piotrowski, 2003. “Identification and characterization of plant
agmatine iminohydrolase, the last missing link in polyamine biosynthesis of plants,” FEBS.
Letters, 544(1–3):258–261.
Jayakannan, M., J. Bose, O. Babourina et al., 2013. “Salicylic acid improves salinity tolerance in
Arabidopsis by restoring membrane potential and preventing salt-inducedK+ loss via aGORK.
channel,” Journal of Experimental Botany, 64(8):2255–2268.
Jeschke, W.D., A.D. Peuke, J.S. Pate, and W. Hartung, 1997. “Transport, synthesis and catabolism of
abscisic acid (ABA) in intact plants of castor bean (Ricinus communis L). under phosphate
deficiency andmoderate salinity,” Journal of Experimental Botany, 48(314):1737–1747,
Jiang, C., M. Johkan, M. Hohjo, S. Tsukagoshi, and T. Maruo, 2017. A correlation analysis on
chlorophyll content and SPAD. value in tomato leaves. Hortic. Res., 71: 37–42.
Jiang, K., C. Schwarzer, E. Lally, S. Zhang, S. Ruzin, T. Machen, S.J. Remington, and L. Feldman,
2006. Expression and characterization of a redox-sensing green fluorescent protein (reduction-
oxidation-sensitive green fluorescent protein. in Arabidopsis. Plant Physiol., 141: 397–403.
[CrossRef] [PubMed]
Jiang, K., J. Moe-Lange, L. Hennet, and L.J. Feldman, 2016. Salt stress affects the redox status of
Arabidopsis root meristems. Front. Plant Sci., 7, 81. [CrossRef] [PubMed]
Jiang, Y., B. Yang, N.S. Harris, and M.K. Deyholos, 2007. Comparative proteomic analysis of NaCl
stress-responsive proteins in Arabidopsis roots. J. Exp. Bot., 58:3591–3607.
Jobe, T.O., I. Zenzen, K.P. Rahimzadeh, and S. Kopriva, 2019. Integration of sulfate assimilation with
carbon and nitrogen metabolism in transition from C3 to C4 photosynthesis. J. Exp. Bot., 70:
4211–4221. [CrossRef]
Juan, M., R.M. Rivero, L. Romero, and J.M. Ruiz, 2005. Evaluation of some nutritional and
biochemical indicators in selecting salt-resistant tomato cultivars. Environ. Exp. Bot. 54: 193–
201. doi: 10.1016/j.envexpbot.2004.07.004
Kalaji, H.M., B.K. Govindjee, J. Koscielniakd, and K. Zük-Gołaszewska, 2011. Effects of salt stress on
photosystem II. efficiency and CO2 assimilation of two Syrian barley landraces. Environ. Exp.
Bot., 73:64–72
Kalaji, H.M., K. Bosa, J. Ko´scielniak, and K. Zuk-Gołaszewska, 2011. Effects of salt stress on
photosystem II. efficiency and CO 2 assimilation of two Syrian barley landraces. Environ. Exp.
Bot., 73:64–72. [CrossRef].
Kamala, G., D. Abhijit and G. Bhaskar 2013. Plant polyamines in abiotic stress responses. Acta Physiol
Plant, DOI. 10.1007/s11738-013-1239-4.
Karunakaran, G., R. Suriyaprabha, P. Manivasakan, R. Yuvakkumar, V. Rajendran, P. Prabu, and N.
Kannan, 2013Effect of nanosilica and silicon sources on plant growth promoting rhizobacteria,
soil nutrients and maize seed germination. IET. Nanobiotechnol., 7:70–77. [CrossRef]
Kaur, G., S. Kumar, H. Nayyar, and H.D. Upadhyaya, 2008. Cold stress injury during the pod-
fillingphase in chickpea (Cicer arietinum L). : effects on quantitative and qualitative
components of seeds. J. Agron. Crop. Sci., 194:457–464.
Kav, N.N.V., S. Srivastava, L. Goonewardende, and S.F. Blade, 2004. Proteome level changes in the
roots of Pisum sativum in response to salinity. Ann. Appl. Biol., 145:217–230.
Kaveh, H., H. Nemati, M. Farsi, and S.V. Jartoodeh, 2011. How salinity affect germination and
emergence of tomato lines. J. Biol. Environ. Sci., 5: 159–163.
Kerepesi, I. and G. Galiba, 2000. “Osmotic and salt stress-induced alteration in soluble carbohydrate
content in wheat seedlings,” Crop Science, 40(2):482–487.

377
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Keskin, B.C., A.T. Sarikaya, B. Y¨uksel, and A.R. Memon, 2010. “Abscisic acid regulated gene
expression in bread wheat (Triticum aestivum L)” Australian Journal of Crop Science,
4(8):617–625.
Keutgen, A.J., and E. Pawelzik 2009. Impacts of NaCl stress on plant growth and mineral nutrient
assimilation in two cultivars of strawberry. Environ Exp. Bot., 65:170–176
Khan M. A., I. A. Ungar, and A. M. Showalter, 2000. “Effects of sodium chloride treatments on growth
and ion accumulation of the halophyte haloxylon recurvum,” Communications in Soil Science
and Plant Analysis, 31(17-18):2763–2774,
Khan, M.A., and D.J. Weber, 2008. Ecophysiology of high salinity tolerant plants (tasks for vegetation
science., 1st edn. Springer, A.msterdam
Khan, M.A., and Y. Rizvi, 1994. Effect of salinity, temperature and growth regulators on the
germination and early seedling growth of Atriplex griffithii var. Stocksii. Can J. Bot., 72:475–
479.
Khan, M.A., I.A. Ungar, and A.M. Showalter, 2000. Effects of salinity on growth, water relations and
ion accumulation of the subtropical perennial halophyte, A.triplex griffithii var. stocksii. Ann.
Bot., 85:225–232.
Khan, M.A., M.U. Shirazi, M.A. Khan, S.M. Mujtaba, E. Islam, S. Mumtaz, et al., 2009. Role of proline,
K./NA. ratio and chlorophyll content in salt tolerance of wheat (Triticum aestivum L). Pakistan
J. Bot. 41: 633–638.
Khan, M.I.R., N. Iqbal, A. Masood, and N.A. Khan, 2012. Variation in salt tolerance of wheat cultivars:
Role of glycinebetaine and ethylene. Pedosphere, 22:746-754.
Khan, M.M., R.S.M. Al-Mas'oudi, F. Al-Said, and I. Khan, 2013. Salinity effects on growth, electrolyte
leakage, chlorophyll content and lipid peroxidation in cucumber (Cucumis sativus L). 2013
International Conference on Food and Agricultural Sciences IPCBEE. vol.55, I.ACSIT. Press,
S.ingapore doi:10.7763/IPCBEE.2013. V55. 6.
Khan, M.N., M. Mobin, Z.K. Abbas, K.A. AlMutairi, and Z.H. Siddiqui, 2017. Role of nanomaterials
in plants under challenging environments. Plant Physiol. Biochem., 110: 194–209.
Khan, M.R., V. Adam, T.F. Rizvi, B. Zhang, F. Ahamad, I. Jo´sko, Y. Zhu, M. Yang, and C. Mao,
2019b. Nanoparticle–plant interactions: two-way traffic. Small 15, 1901794.
Khanna-Chopra, R., K.S. Vimal, L. Nita, and P. Ashwani, 2019. Proline – A. Key Regulator Conferring
Plant Tolerance to Salinity and Drought, C.hapter 5, DOI: 10.1201/9780203705315-5.
Khodarahmpour, Z., M. Ifar, and M. Motamedi, 2012. Effects of NaCl salinity on maize (Zea mays L).
at germination and early seedling stage. Afr. J. Biotechnol., 11:298–304.
Kibria, M.G. and H.Md.Anamul, 2019. A Review on Plant Responses to Soil Salinity and Amelioration
Strategies, D.OI: 10.4236/ojss. 911013 Nov. 1, O.pen Journal of Soil Science.
Kibria, M.G., M.A. Hossain, Y. Murata, and M.A. Hoque, 2017. Antioxidant Defense Mechanisms of
Salinity Tolerance in Rice Genotypes. Rice Science, 24: 155-162.
https://doi.org/10.1016/j.rsci.2017.05.001
Kilili, K.G., N. Atanassova, A. Vardanyan, N. Clatot, K. Al-Sabarna, P.N. Kanellopoulos, A.M. Makris,
and S.C. Kampranis, 2004. Differential roles of tau class glutathione S-transferases in oxidative
stress. J. Biol. Chem., 279, 24540–24551. [CrossRef] [PubMed]
Kim, D.W., R. Rakwal, G.K. Agrawal, Y.H. Jung, J. Shibato, N.S. Jwa, Y. Iwahashi, H. Iwahashi, D.H.
Kim, I.S. Shim, K. Usui 2005. A. hydroponic rice seedling culture model system for
investigating proteome of salt stress in rice leaf. Electrophoresis, 26:4521–4539.
Kim, S.H., D.H. Woo, J.M. Kim, S.Y. Lee, W.S. Chung, and Y.H. Moon, 2011. Arabidopsis MKK4
mediates osmotic-stress response via its regulation of MPK3 activity. Biochem Biophys Res
Commun 412:150– 154
Kim, Y.H., A. Latif Khan, M. Waqas et al., 2013. “Silicon application to rice root zone influenced the
phytohormonal and antioxidant responses under salinity stress,” Journal of Plant Growth
Regulation,
Kim, Y.H., A.L. Khan, M. Waqas, J.K. Shim, D.H. Kim, K.Y. Lee, and I.J. Lee, 2014. Silicon
application to rice root zone influenced the phytohormonal and antioxidant responses under
salinity stress. J. Plant Growth Regul., 33: 137–149.

378
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Kim, Y.H., A.L. Khan, M. Waqas, J.K. Shim, D.H. Kim, K.Y. Lee, and I.J. Lee, 2014. Silicon
application to rice root zone influenced the phytohormonal and antioxidant responses under
salinity stress. J. Plant Growth Regul., 33: 137–149. [CrossRef]
Kinoshita, J.H., 1990. A thirty year journey in the polyol pathway. Exp. Eye. Res., 50(6):567–573.
https://doi.org/10.1016/0014-4835 (90) 90096-D.
Knott, J.M., P. R¨omer, and M. Sumper, 2007. “Putative spermine synthases from Thalassiosira
pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine,” FEBS.
Letters, 581(16):3081–3086.
Kocsy, G., I. Tari, R. Vanková, B. Zechmann, Z. Gulyás, P. Poór, and G. Galiba, 2013. Redox control
of plant growth and development. Plant Sci., 211:77–91. PMID: 23987814.
doi:10.1016/j.plantsci.2013.07.004.
Kopriva, S., 2006. Regulation of sulfate assimilation in Arabidopsis and beyond. Ann Bot 97: 479-495.
Kopriva, S., and H. Rennenberg, 2004. Control of sulphate assimilation and glutathione synthesis:
interaction with N. and C. metabolism. J. Exp. Bot., 55: 1831- 1842.
Koprivova, A., and S. Kopriva, 2008. Lessons from investigation of regulation of APS. reductase by
salt stress. Plant Signal. Behav. 3: 567-569.
Kopyra, M. and E.A. Gw´o´zd´z, 2003. “Nitric oxide stimulates seed germination and counteracts the
inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus,” Plant
Physiology and Biochemistry, 41(11-12):1011–1017.
Kosová, K., I.T. Prášil, and P. Vítámvás, 2013. Protein contribution to plant salinity response and
tolerance acquisition a review. Int. J. Mol. Sci., 14:6757–6789.
Kosová, K., P. Vítámvás, and I.T. Prášil, 2010. The role of dehydrins in plant stress response.
In:Handbook of Plant and CropStress. Pessarakli M. (ed.) CRC. Press, T.aylor and Francis:
Boca Raton, FL, USA, 239– 285.
Kosova, K., P.V. ´ ´ıtamv ´ as, I.T. Pr ´ a´ˇsil, and J. Renaut, 2011. “Plant proteome changes under
abiotic stress—contribution of proteomics studies to understanding plant stress response,”
Journal of Proteomics, 74(8):1301–1322.
Kov´acs, Z., L. Simon-Sarkadi, A. Szucs, and G. Kocsy, 2010. “Differential effects of cold, osmotic
stress and abscisic acid on polyamine accumulation inwheat,”Amino Acids, 38(2):623–631.
Krueger, S., A. Donath, M.C. Lopez-Martin, R. Hoefgen, C. Gotor, et al., 2010. Impact of sulfur
starvation on cysteine biosynthesis in T-DNA. mutants deficient for compartment-specific
serine-acetyltransferase. Amino Acids, 39: 1029-1042.
Kumar, D., and S. Chattopadhyay, 2018. Glutathione modulates the expression of heat shock proteins
via the transcription factors BZIP10 and MYB21 in Arabidopsis. J. Exp. Bot., 69: 3729–3743.
[CrossRef]
Kumar, G., R.S. Purty, M.P. Sharma, S.L. Singla-Pareek, and A. Pareek, 2009. Physiological responses
among Brassica species under salinity stress show strong correlation with transcript abundance
for SOS. pathway-related genes. J. Plant Physiol., 166:507–520.
Kumar, M., H. Etesami, and V. Kumar, 2019. Saline Soil-based Agriculture by Halotolerant
Microorganisms. Springer. Kumar, V., G.uleria, P., K.umar, V., Y.adav, S.K., 2013. Gold
nanoparticle exposure induces growth and yield enhancement in Arabidopsis thaliana. Sci.
Total Environ. 461–462, 462–468.
Kumar, N.C., K.L. Milan, K.T. Rahul, D. Devanshu, B.K. Hemant, U.P. Virupaksh, K. Amarjeet, V.
Girimalla, K. Dharmendra, B. Vinay, K.M. Jitendra, M. Vikas, M.S. Rahul, K. Jae-Yean and
P. Dibyajyoti, 2021. Salinity Stress in Potato: Understanding Physiological, B.iochemical and
Molecular Responses, L.ife 2021, 11, 545. https://doi.org/10.3390/life11060545
https://www.mdpi.com/journal/life
Kumar, S.A., S.I. Alam, N. Sengupta, and R. Sarin, 2011. Differential proteomic analysis of salt
response in Sorghum bicolor leaves. Environ. Exp. Bot., 71:321–328.
Kumari, S., V. Panjabi, H.R. Kushwaha, S.K. Sopory, S.L. Singla-Pareek, and A. Pareek, 2009.
Transcriptome map for seedling stage specific salinity stress response indicates a specific set of
genes as candidate for saline tolerance in Oryza sativa L. Funct Integr Genomics, 9:109–123.
Kurth, E., G.R. Cramer, A. Lauchli, and E. Epstein, 1986. Effects of NaCl and CaCl2 on cell
enlargement and cell production in cotton roots. Plant Physiol., 82:1102–1106.

379
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Kusano, T., K. Yamaguchi, T. Berberich, and Y. Takahashi, 2007. “Advances in polyamine research in
2007,” Journal of Plant Research, 120(3):345–350.
Kyriakis, J.M., and J. Avruch, 2012. Mammalian MAPK. Signal transduction pathways activated by
stress and inflammation: a 10-year update. Physiol. Rev., 92:689–737.
Laane, H., 2017. The effects of the application of foliar sprays with stabilized silicic acid: An overview
of the results from 2003-2014. Silicon-Neth., 9: 803–807. [CrossRef]
Laane, H., 2018. The effects of foliar sprays with diferent silicon compounds. Plants, 7, 45. [CrossRef]
[PubMed].
Lancaster, J.R., 2015. Nitric oxide: A. brief overview of chemical and physical properties relevant to
therapeutic applications. Future Sci. OA, 1. [CrossRef]
Lappartient, A.G., and B. Touraine, 1996. Demand-Driven Control of Root ATP. Sulfurylase Activity
and SO42- Uptake in Intact Canola (The Role of PhloemTranslocated Glutathione. Plant
Physiol., 111: 147-157.
Latef, A.A.H.A., M.FA. Ahmed, and K.E. Abdel Fattah, 2017. The possible roles of priming with ZnO.
nanoparticles in mitigation of salinity stress in lupine (Lupinus termis) plants. J. Plant Growth
Regul., 36(1):60–70. https://doi.org/10.1007/s00344-016-9618-x
Lauchli, A., and S.R. Grattan, 2007. Plant growth and development under salinity stress. In: Jenks MA,
H.asegawa PM, Mohan JS. (eds) Advances in molecular breeding towards drought and salt
tolerant crops. Springer, B.erlin, 1–32.
Lawlor, D.W. 2009. Musings about the effects of environment on photosynthesis. Ann. Bot. 103: 543–
549. doi: 10.1093/aob/mcn256
Lea-Cox, J.D., and J.P. Syvertsen, 1993. Salinity reduces water use and nitrate- N-use efficiency of
citrus. Ann. Bot., 72:47–54
Lee, S.M., E.J. Lee, E.J. Yang, J.E. Lee, A.R. Park, W.H. Song, and O.K. Park, 2004b. Proteomic
identification of annexins, calcium-dependent membrane binding proteins that mediateosmotic
stress and abscisic acid signal transduction in Arabidopsis. Plant Cell, 16:1378–1391.
Lee, Y.S., S.R. Park, H.J. Park, and Y.W. Kwon, 2004a. Salt stress magnitude can be quantified by
integrating salinity with respect to duration. Proceedings of 4th International Crop Sci.
Congress. Brisbane, Aust 26 Sept-1 Oct pp 1–5.
Leustek, T., M.N. Martin, J.A. Bick, and J.P. Davies, 2000. Pathways And Regulation Of Sulfur
Metabolism Revealed Through Molecular And Genetic Studies. Annu. Rev. Plant Physiol Plant
Mol. Biol., 51: 141-165.
Li, B., L. He, S. Guo et al., 2013. “Proteomics reveal cucumber Spd-responses under normal condition
and salt stress,” Plant Physiology and Biochemistry, 67:7–14.
Li, H., J. Chang, H. Chen, Z. Wang, X. Gu, C. Wei, Y. Zhang, J. Ma, J. Yang, and X. Zhang, 2017.
Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis
and redox homeostasis. Front. Plant Sci., 8: 295. [CrossRef]
Li, H., Y. Dong, H. Yin, N. Wang, J. Yang, X. Liu, Y. Wang, J. Wu, and X. Li 2011a. Characterization
of the stress associated micro RNAs in Glycine max by deep sequencing. BMC. Plant Biol.
11:170.
Li, H., Y. Zhu, Y. Hu, W. Han, and H. Gong, 2015. “Beneficial effects of silicon in alleviating salinity
stress of tomato seedlings grown under sand culture,” Acta Physiologiae Plantarum, 37(4):1–9.
Li, H., Y. Zhu, Y. Hu, W. Han, and H. Gong, 2015. Beneficial effects of silicon in alleviating salinity
stress of tomato seedlings grown under sand culture. Acta Physiol. Plant., 37, 71. [CrossRef]
Li, J., G. Brader, E. Helenius, T. Kariola, and E.T. Palva, 2012. Biotin deficiency causes spontaneous
cell death and activation of defense signaling. Plant J. 70: 315- 326.
Li, Q., G. Yan and Y. An, 2020. Sulfur Homeostasis in Plants, Int. J. Mol. Sci., 21, 8926; doi:
10.3390/ijms21238926 www.mdpi.com/journal/ijms
Li, T.X.Y.Z., Y. Zhang, H. Liu, Y.T. Wu, W.L. Bin, and H.X. Zhang, 2010. Stable expression of
arabidopsis vacuolar Na+/H+ antiporter gene AtNHX1, and salt tolerance in transgenic soybean
for over six generations. Chinese Sci. Bull., 55: 1127–1134. doi: 10.1007/s11434-010-0092-8.
Li, W., C. Zhang, Q. Lu, X. Wen, and C. Lu 2011b. The combined effect of salt stress and heat shock
on proteome profiling in Suaeda salsa. J. Plant Physiol., 168:1743–1752.

380
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Li, Y., W. Zhang, J. Cui, D. Lang, M. Li, Q. Zhao, and X. Zhang, 2016 Silicon nutrition alleviates the
lipid peroxidation and ion imbalance of Glycyrrhiza uralensis seedlings under salt stress. Acta
Physiol. Plant, 38, 96. [CrossRef]
Liang, X., H. Wang, Y. Hu, L. Mao, L. Sun, T. Dong, W. Nan, and Y. Bi, 2015Silicon does not mitigate
cell death in cultured tobacco BY-2 cells subjected to salinity without ethylene emission. Plant
Cell Rep., 34: 331–343. [CrossRef] [PubMed]
Liang, Y., 1999. Effects of silicon on enzyme activity and sodium, potassium and calcium concentration
in barley under salt stress. Plant Soil, 209: 217–224. [CrossRef]
Liang, Y., Q. Chen, Q. Liu, W. Zhang, and R. Ding, 2003Exogenous silicon (Si. increases antioxidant
enzyme activity and reduces lipid peroxidation in roots of salt-stressed barley (Hordeum
vulgare L). J. Plant Physiol., 160: 1157–1164. [CrossRef] [PubMed]
Liang, Y., W. Sun, Y.G. Zhu and P. Christie, 2007. Mechanisms of silicon-mediated alleviation of
abiotic stresses in higher plants: a review. Environ. Pollut., 147: 422-428
Liang, Y., W. Zhang, Q. Chen, R. Ding, 2005. Effects of silicon on H+-ATPase and H+-PPase activity,
fatty acid composition and fluidity of tonoplast vesicles from roots of salt-stressed barley
(Hordeum vulgare L). Environ. Exp. Bot., 53: 29–37. [CrossRef]
Liang, Y., W. Zhang, Q. Chen, Y. Liu, and R. Ding, 2006. Effect of exogenous silicon (Si. on H+-
ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed
barley (Hordeum vulgare L). Environ. Exp. Bot., 57: 212–219. [CrossRef]
Lin, H., Y. Yang, R. Quan, I. Mendoza, Y. Wu, W. Du, S. Zhao, K.S. Schumaker, J.M. Pardo, and Y.
Guoa, 2009. Phosphorylation of SOS3-like calcium binding protein8 by SOS2 protein kinase
stabilizes their protein complex and regulates salttolerance in Arabidopsis. Plant Cell, 21: 1607–
1619.
Linghe, Z., and M.C. Shannon, 2000. Salinity effects on seedling growth and yield components of rice.
Crop Sci., 40:996–1003.
Liska, A.J., A. Shevchenko, U. Pick, and A. Katz, 2004. Enhanced photosynthesis and redox energy
production contribute to salinity tolerance in Dunaliella as revealed by homology-based
proteomics. Plant Physiol., 136:2806–2817.
Liu, H.H., X. Tian, Y.J. Li, C.A. Wu, and C.C. Zheng, 2008. Microarray-based analysis of stress-
regulated microRNAs in Arabidopsis thaliana. RNA. 14:836–843.
Liu, J., M. Ishitani, U. Halfter, C.-S. Kim, and J.-K. Zhu, 2000. “The Arabidopsis thaliana SOS2 gene
encodes a protein kinase that is required for salt tolerance,” Proceedings of the National
Academy of Sciences of theUnited States ofAmerica, 97(7):3730– 3734.
Liu, J., M. Ishitani, U. Halfter, C.S. Kim, J.K. Zhu. 2000. The Arabidopsis thaliana SOS2 gene encodes
a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA. 97:3730–3734.
Liu, J.H., W. Wang, H. Wu, X. Gong, and T. Horiguchi, 2015. Polyamines function in stress tolerance:
from synthesis to regulation. Front Plant Sci., 6:827. https://doi.org/10.3389/fpls.2015.00827.
Liu, P., L. Yin, S. Wang, M. Zhang, X. Deng, and S. Zhang, 2015. Enhanced root hydraulic conductance
by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress in Sorghum
bicolor L. Environ. Exp. Bot. 111:42–51. doi: 10.1016/j.envexpbot.2014.10.006
Liu, P., L. Yin, S. Wang, M. Zhang, X. Deng, S. Zhang, and K. Tanaka, 2015Enhanced root hydraulic
conductance by aquaporin regulation accounts for silicon alleviated salt-induced osmotic stress
in Sorghum bicolor L. Environ. Exp. Bot., 111: 42–51. [CrossRef]
Liu, P., L. Yin, X. Deng, S. Wang, K. Tanaka, and S. Zhang, 2014. Aquaporin-mediated increase in
root hydraulic conductance is involved in silicon-induced improved root water uptake under
osmotic stress in Sorghum bicolor L. J. Exp. Bot., 65: 4747–4756. [CrossRef]
Liu, R., and R. Lai, 2015. Potentials of engineered nanoparticles as fertilizers for increasing agronomic
productions. Sci. Total Environ., 51:131–139.
Localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol. Biol., l26:1921–1934.
López-Berenguer, C., M.C. Martínez-Ballesta, C. García-Viguera, and M. Carvajal, 2008. Leaf water
balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in
broccoli. Plant Sci., 174: 321-328.
López-Berenguer, C., M.C. Martínez-Ballesta, D.A. Moreno, M. Carvajal, and C. GarcÃa-Viguera,
2009. Growing hardier crops for better health: Salinity tolerance and the nutritional value of
broccoli. J. Agric. Food Chem., 57: 572-578.

381
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Lòpez-Climent, M.F., V. Arbona, R.M. Pérez-Clemente, and A. Gòmez-Cadenas, 2008. Relationship

between salt tolerance and photosynthetic machinery performance in citrus. Environ. Exp. Bot.,
62:176–184.
López-Martín, M.C., L.C. Romero, and C. Gotor, 2008. Cytosolic cysteine in redox signaling. Plant
Signal Behav., 3: 880-881.
Lopez-Martin, M.C., M. Becana, L.C. Romero, and C. Gotor 2008a. Knocking out cytosolic cysteine
synthesis compromises the antioxidant capacity of the cytosol to maintain discrete
concentrations of hydrogen peroxide in Arabidopsis. Plant Physiol., 147: 562-572.
Lotfi, R., and K. Ghassemi-Golezani, 2015. Influence of salicylic acid and silicon on seed development
and quality of mung bean under salt stress. Seed Sci. Technol., 43: 52–61. [CrossRef]
Lu, C., C. Mo-Xian, L. Rui, Z. Lin, H. Xuanxuan, L. Shouxu, D. Xinhua, J. Yong, X. Jiandi, Z. Jianhua,
Z. Xiangyu and L. Ying-Gao, 2019.Abscisic Acid Regulates Auxin Distribution to Mediate
Maize Lateral Root Development Under Salt, F.rontiers in Plant Science | www.frontiersin.org,
10(716).
Lu, S.F., Y.H. Sun, and V.L. Chiang, 2008. Stress-responsive microRNAs in Populus. Plant J., 55:131–
151.
Lu, Y., H. Lam, E. Pi, Q. Zhan, S. Tsai, C. Wang, Y. Kwan, and S. Ngai, 2013. Comparative
metabolomics in Glycine max and Glycine soja under salt stress to reveal the phenotypes of
their offspring. J. Agric. Food Chem., 61:8711–8721.
Luyckx, M., J.F. Hausman, S. Lutts, and G. Guerriero, 2017. Silicon and plants: Current knowledge
and technological perspectives. Front. Plant Sci., 8, 411. [CrossRef]
Ma, J.F., 2002. Arice mutant defective in Si uptake. Plant Physiol., 130: 2111–2117. [CrossRef]
[PubMed]
Ma, J.F., and N. Yamaji, 2015. A cooperative system of silicon transport in plants. Trends Plant Sci.
20: 435–442. Doi: 10.1016/j.tplants.2015.04.007.
Ma, L., H. Zhang, L. Sun et al., 2012. “NADPH. oxidase Atrboh D. and Atrboh F. function in ROS-
dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress,” Journal of
Experimental Botany, 63(1):305–317.
Ma, Y., L. Kuang, X. He, W. Bai, Y. Ding, Z. Zhang, Y. Zhao, and Z. Chai, 2010. Effects of rare earth
oxide nanoparticles on root elongation of plants. Chemosphere, 78: 273–279.
Mahajan, S., G.K. Pandey, and N. Tuteja 2008. Calcium and salt-stress signaling in plants: shedding
light on SOS. pathway. Arch. Biochem. Biophys., 471:146–158.
Mahdieh, M., N. Habibollahi, M.R. Amirjani, M.H. Abnosi, and M. Ghorbanpour, 2015. Exogenous
silicon nutrition ameliorates saltinduced stress by improving growth and efficiency of PSII. in
Oryza sativa L. cultivars. J. Soil Sci. Plant Nutr., 15: 1050–1060. [CrossRef]
Makela, P., J. Karkkainen, and S. Somersalo, 2000. “Effect of glycinebetaine on chloroplast
ultrastructure, chlorophyll and protein content, and RuBPCO. activities in tomato grown under
drought or salinity,” Biologia Plantarum, 43(3):471– 475.
Malakar, P. and D. Chattopadhyay, 2021. Adaptation of plants to salt stress: the role of the ion
transporters, J.ournal of Plant Biochemistry and Biotechnology, 30(4):668–683
https://doi.org/10.1007/s13562-021-00741-6
Manaa, A., H.B. Ahmed, B. Valot, J.P. Bouchet, S. Aschi-Smiti, M. Causse, and M. Faurobert, 2011.
Salt and genotype impact on plant physiology and root proteome variations in tomato. J. Exp.
Bot. 62:2797–2813.
Mane, A.V., B.A. Karadge, and J.S. Samant, 2010. Salinity induced changes in photosynthetic pigments
and polyphenols of Cymbopogon Nardus (L). Rendle. J. Chem. Pharm. Res., 2:338–347.
Mantri, N., V. Patade, S. Penna, R. Ford, and E. Pang, 2012. Abiotic stress responses in plants: present
and future. In: Ahmad P, Prasad MNV. (eds) Abiotic stress responses in plants: metabolism,
productivity and sustainability. Springer, N.ew York, 1–19.
Marchal, C., V. Delorme-Hinoux, L. Bariat, W. Siala, C. Belin, J. SaezVasquez, C. Riondet, J.P.
Reichheld, 2014. NTR/NRX. define a new thioredoxin system in the nucleus of Arabidopsis
thaliana cells. Mol Plant. 7:30–44. PMID: 24253198. doi:10.1093/mp/ sst162.
Maron, L.G., 2019. From foe to friend: The role of chloride as a beneficial macronutrient. Plant J., 99:
813–814. [CrossRef] [PubMed]

382
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Marschner, H., 1995. “Functions of mineral nutrients: macronutrients,” in Mineral Nutrition of Higher
Plants, H. Marschner, (Ed.). 379–396, G.ulf Professional Publishing, Houston, Tex, U.SA, 2nd
edition,
Mart´ınez-Atienza, J., X. Jiang, B. Garciadeblas et al., 2007. “Conservation of the salt overly sensitive
pathway in rice,” Plant Physiology, 143(2):1001–1012.
Martí, M.C., E. Olmos, J.J. Calvete, I. Díaz, S. Barranco-Medina, J. Whelan, J.J. Lázaro, F. Sevilla,
and A. Jiménez, 2009. Mitochondrial and nuclear localization of a novel pea thioredoxin:
identification of its mitochondrial target proteins. Plant Physiol., 150:646–657. PMID:
19363090. doi:10.1104/pp.109.138073.
Martí, M.C., I. Florez-Sarasa, D. Camejo, M. Ribas-Carbó, J.J. Lázaro, et al., 2011. Response of
mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to salinity in pea
(Pisum sativum L). leaves. J. Exp. Bot., 62: 3863- 3874.
Martí, M.C., I. Florez-Sarasa, D. Camejo, M. Ribas-Carbó, J.J. Lázaro, F. Sevilla, and A. Jiménez,
2011. Response of mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to
salinity in pea (Pisum sativum L). leaves. J. Exp. Bot., 62:3863–3874. PMID: 21460385.
doi:10.1093/jxb/err076.
Martínez-Atienza, J., X. Jiang, B. Garciadeblas, I. Mendoza, J.K. Zhu, J.M. Pardo, and F.J. Quintero,
2007. Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012
Martínez-Ruiz, A., S. Cadenas, and S. Lamas, 2011. Nitric oxide signaling: Classical, less classical and
nonclassical mechanisms. Free Radic. Biol. Med., 51: 17–29. [CrossRef]
Mass, E.V., 1986. Salt tolerance of plants. Appl. Agric. Res., 1:12–26.
Mastronardi, E., P. Tsae, X. Zhang, C.M. Monreal, and M.C. DeRosa, 2015. Strategic role of
nanotechnology in fertilizers: potential and limitations. In: Rai M, Ribeiro C, Mattoso L, D.uran
N. (eds) Nanotechnologies in food and agriculture. Springer, Berlin.
Mathebula, S.D., 2015. Polyol pathway: A. possible mechanism of diabetes complications in the eye.
Afr Vis Eye Health., 74 (1):a13. https://doi.org/10.4102/aveh. v74i1.13.
Matoh, T., P. Kairusmee, and E. Takahashi, 1986. Salt-induced damage to rice plants and alleviation
effect of silicate. Soil Sci. Plant Nutr., 32: 295–304. [CrossRef]
Matysik, J., A. Alia, B. Bhalu, and P. Mohanty, 2002. “Molecular mechanisms of quenching of reactive
oxygen species by proline under stress in plants,” Current Science, 82(5):525– 532.
May, M.J., T. Vernoux, C. Leaver, M. Van Montagu, and D. Inze, 1998. Glutathione homeostasis in
plants: implications for environmental sensing and plant development. J. Exp. Bot., 49: 649-
667.
Mendoza, I., F. Rubio, A. Rodriguez-Navarro, and J.M. Pardo, 1994. The protein phosphatise
calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J. Biol. Chem.,
269:8792–8796.
Meng, L., J.H. Wong, L.J. Feldman, P.G. Lemaux, and B.B. Buchanan, 2010. A. membrane-associated
thioredoxin required for plant growth moves from cell to cell, suggestive of a role in
intercellular communication. Proc Natl Acad Sci USA., 107:3900–3905. PMID: 20133584.
doi:10.1073/pnas.0913759107.
Merrick, B.A., and M.E. Bruno, 2004. Genomic and proteomic profiling for biomarkers and signature
profiles of toxicity. Curr. Opin. Mol. Ther., 6:600–607.
Meyer, A.J., and R. Hell, 2005. Glutathione homeostasis and redox-regulation by sulfhydryl groups.
Photosynth Res., 86: 435-457.
Mir, R.A., A.B. Basharat, Y. Henan, T.I. Sheikh, R. Ali, A.R. Masood, C. Sidra, A. Mohammed, A.S.
Parvaze and M.Z. Sajad, 2022. Multidimensional Role of Silicon to Activate Resilient Plant
Growth and to Mitigate Abiotic Stress, F.rontiers in Plant Science | www.frontiersin.org, 13 :
819658.
Mishra, S., A.B. Jha, and R.S. Dubey, 2011. “Arsenite treatment induces oxidative stress, upregulates
antioxidant system, and causes phytochelatin synthesis in rice seedlings,” Protoplasma,
248(3):565–577.
Mittal, D., K. Gurjeet, S. Parul, Y. Karmveer and A.A. Syed, 2020. Nanoparticle-Based Sustainable
Agriculture and Food Science: Recent Advances and Future Outlook, Frontiers in
Nanotechnology | www.frontiersin.org, 2:579954.

383
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Mittal, S., N. Kumari, and V. Sharma, 2012. Differential response of salt stress on Brassica juncea:
photosynthetic performance, pigment, proline, D.1 and antioxidant enzymes. Plant Physiol.,
Biochem., 54:17–26.
Mittal, S., N. Kumari, and V. Sharma, 2012. Differential response of salt stress on Brassica juncea:
photosynthetic performance, pigment, proline, D.1 and antioxidant enzymes. Plant Physiol.
Biochem. 54: 17–26. doi: 10.1016/j.plaphy.2012.02.003.
Mittler, R. and E. Blumwald, 2015. The roles of ROS. and ABA. in systemic acquired acclimation.
Plant Cell, 27: 64–70.
Mittler, R., S. Vanderauwera, M. Gollery, and F. Van Breusegem, 2004 Reactive oxygen gene network
of plants. Trends Plant Sci., 9: 490–498. [CrossRef]
Mittova, V., F.L. Theodoulou, G. Kiddle, L. Gómez, M. Volokita, et al., 2003. Coordinate induction
of glutathione biosynthesis and glutathione-metabolizing enzymes is correlated with salt
tolerance in tomato. FEBS. Lett., 554: 417-421.
Mittova, V., M. Guy, M. Tal, and M. Volokita, 2004. Salinity upregulates the antioxidative system in
rootmitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon
pennellii. J. Exp. Bot., 55:1105–1113.
Molassiotis, A.N., T. Sotiropoulos, G. Tanou, G. Kofidis, G. Diamantidis and I. Therios, 2006.
Antioxidant and anatomical responses in shoot culture of the apple rootstock MM. 106 treated
with NaCl, K.Cl, mannitol or sorbitol. Biol. Plant, 50: 61-68
Moln´ar, ´A., M. Papp, D. Zolt´an Kov´acs, P. B´elteky, D. Ol´ah, G. Feigl, R. Sz˝oll˝osi, Z. R´azga,
A. ¨Ord¨og, L. Erdei, A. R´onav´ari, Z. K´onya, and Z. Kolbert, 2020. Nitro-oxidative signalling
induced by chemically synthetized zinc oxide nanoparticles (ZnO) NPs. in Brassica species.
Chemosphere, 251: 126419.
Monirifar, H., and M. Barghi, 2009. Identification and selection for salt tolerance in alfalfa (Medicago
sativa L). ecotypes via physiological traits. Not. Sci. Biol. 1: 63–66. doi: 10.15835/nsb113498
Montrichard, F., F. Alkhalfioui, H. Yano, W.H. Vensel, W.J. Hurkman, and B.B. Buchanan, 2009.
Thioredoxin targets in plants: the first 30 years. J. Proteomics., 72:452–474. PMID:
19135183.doi:10.1016/j. jprot.2008.12.002.
Moon, H., B. Lee, G. Choi, S. Shin, D.T. Prasad, O. Lee, S.S. Kwak, D.H. Kim, J. Nam, J. Bahk, J.C.
Hong, S.Y. Lee, M.J. Cho, C.O. Lim, and D.J. Yun, 2003. NDP. kinase 2 interacts with two
oxidative stress-acivated MAPKs to regulate cellular redox state and enhancesmultiple stress
tolerance in transgenic plants. Proc. Natl. Acad. Sci., U. S. A., 100:358–363.
Moons, A., G. Bauw, E. Prinsen, M. van Montagu, and D. van Der Straeten, 1995. Molecular and
physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant
Indica rice varietites. Plant Physiol., 107:177–186
Moradbeygi, H., R. Jamei, R. Heidari, and R. Darvishzadeh, 2020. Investigating the enzymatic and
non-enzymatic antioxidant defense by applying iron oxide nanoparticles in Dracocephalum
moldavica L. plant under salinity stress. Sci. Hortic., 272: 109537.
Moschou, P.N., K.A. Paschalidis, and K.A. Roubelakis- Angelakis, 2008. “Plant polyamine catabolism:
the state of the art,” Plant Signaling and Behavior, 3(12):1061–1066.
Moss, J., and M.D. Lane, 1971. The biotin-dependent enzymes. Adv. Enzymol. Relat Areas Mol. Biol.,
35: 321-442.
Muchate, N.S., C.N. Ganesh, S.R. Nilima, P. Suprasanna and D.N. Tukaram, 2016. Plant Salt Stress:
Adaptive Responses, T.olerance Mechanism and Bioengineering for Salt Tolerance, Bot. Rev.
82:371–406 DOI. 10.1007/s12229-016-9173-y
Muhammad, I., S. Abdullah, A. Muhammad, Y. Qing-Hua, A. Husain and B.L. Feng, 2021.
Mechanisms Regulating the Dynamics of Photosynthesis Under Abiotic Stresses, F.rontiers in
Plant Science | www.frontiersin.org, 11:615942.
Müller, J., M. Beck, U. Mettbach, G. Komis, G. Hause, D. Menzel, and J. Samaj, 2010. Arabidopsis
MPK6 is involved in cell division plane control during early root development, and localizes to
the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J.
61:234–248.
Muneer, S., Y.G. Park, A. Manivannan, P. Soundararajan, and B.R. Jeong, 2014. Physiological and
proteomic analysis in chloroplasts of Solanum lycopersicum L. under silicon efficiency and
salinity stress. Int. J. Mol. Sci. 15: 21803–21824.

384
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Munir N. and F. Aftab, 2011. “Enhancement of salt tolerance in sugarcane by ascorbic acid
retreatment,” African Journal of Biotechnology, 10(80):18362–18370.
Munns R. and M. Tester, 2008. “Mechanisms of salinity tolerance,” Annual Review of Plant Biology,
59:651–681.
Munns R. and M. Tester, 2008. “Mechanisms of salinity tolerance,” Annual Review of Plant Biology,
59:651–681
Munns R., 1993. Physiological processes limiting plant growth in saline soil:some dogmas and
hypotheses. Plant Cell Environ., 16:15–24.
Munns R., 1993. Physiological processes limiting plant growth in saline soils: some dogmas and
hypotheses. Plant Cell Environ., 16:15–24.
Munns R., 2005. Genes and salt tolerance: bringing them together. New Phytol., 167:645–663.
Munns R., and M. Gilliham, 2015. Salinity tolerance of crops – what is the cost? New Phytologist, 208:
668–673.
Munns, R., 2002. Comparative physiology of salt and water stress. Plant Cell Environ., 25:239–250.
Munns, R., 2005. “Genes and salt tolerance: bringing them together,” New Phytologist, 167(3):645–
663.
Munns, R., and M. Gilliham, 2015. Salinity tolerance of crops what is the cost? New Phytol.,
208(3):668–673.
Munns, R., and M. Tester, 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59: 651-
681.
Munns, R., and M. Tester, 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59: 651–
681. [CrossRef]
Muranaka, S., K. Shimizu, and M. Kato, 2002. Ionic and osmotic effects of salinity on single-leaf
photosynthesis in two wheat cultivars with different drought tolerance. Photosynthetica, 40:
201–207. doi: 10.1023/A:1021337 522431
Murty, P.S.S., and K.S. Murty, 1982. Spikelet sterility in relation to nitrogen and carbohydrate contents
in rice. Ind. J. Plant Physiol., 25:40–48.
Musa, A. and M. Sowbiya, 2021. Silicon Supplementation Modulates Physiochemical Characteristics
to Balance and Ameliorate Salinity Stress in Mung Bean.
Naderi, M.R., and A. Danesh-Shahraki, 2013. Nanofertilizers and their roles in sustainable agriculture.
Int J. Agric. Crop Sci., 5:2229–2232.
Nahar, K., and M. Hasanuzzaman, 2009. Germination, growth, nodulation and yield performance of
three mung bean varieties under different levels of salinity stress. Green Farming, 2:825–829.
Najafpour, M.M., M.Z. Ghobadi, A.W. Larkum, J.R. Shen, and S.I. Allakhverdiev, 2015. The biological
water-oxidizing complex at the nano-bio interface. Trends Plant Sci. 20: 559–568. doi:
10.1016/j.tplants.2015.06.005.
Nalousi, A.M., S. Ahmadiyan, A. Hatamzadeh, and M. Ghasemnezhad, 2012. “Protective role of
exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper (Capsicum
annum L).,” American-Eurasian Journal of Agricultural & Environmental Science, 12(8):1085–
1090.
Navakoudis, E., C. L¨utz, C. Langebartels, U. L¨utz-Meindl, and K. Kotzabasis, 2003. “Ozone impact
on the photosynthetic apparatus and the protective role of polyamines,” Biochimica et
Biophysica Acta—General Subjects, 1621(2):160–169.
Navari-Izzo, F., M.F. Quartacci, and S.gherri, 2002. Lipoic acid: a unique antioxidant in the
detoxification of activated oxygen species. Plant Physiol. Biochem., 40: 463-470.
Navari-Izzo, F., R. Izzo, and M.F. Quartacci, 1988. Phospholipid and sterol alterations associated with
salinity and water stress in maize roots. Plant Physiol (Life Science Advance). 7: 137-142.
Navarro, L., P. Dunoyer, and F. Jay, 2006. A. plant miRNA. Contributes to antibacterial resistance by
repressing auxin signaling. Science, 312: 436–439.
Nazar, R., N. Iqbal, A. Masood, S. Syeed, and N.A. Khan, 2011. Understanding the significance of
sulfur in improving salinity tolerance in plants. Environ. Exp. Bot., 70: 80-87.
Nazar, R., N. Iqbal, S. Syeed, and N.A. Khan, 2011. “Salicylic acid alleviates decreases in
photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant
metabolism differentially in two mungbean cultivars,” Journal of Plant Physiology,
168(8):807–815.

385
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Nazar, R., N. Iqbal, S. Syeed, and N.A. Khan, 2011. Salicylic acid alleviates decreases in photosynthesis
under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism
differentially in two mungbean cultivars. J. Plant Physiol., 168: 807-815.
Nazar, R., N. Iqbal, S. Syeed, and N.A. Khan, 2011. Salicylic acid alleviates decreases in photosynthesis
under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism
differentially in two mungbean cultivars. J. Plant Physiol., 168: 807–815. [CrossRef]
[PubMed].
Ndimba, B.K., S. Chivasa, W.J. Simon, and A.R. Slabas, 2005. Identification of Arabidopsis salt and
osmotic stress responsive proteins using two dimensional difference gel electrophoresis and
mass spectrometry. Proteomics, 5:4185–4196.
Nietzel, T. J. Mostertz, F. Hochgräfe, and M. Schwarzländer, 2017. Redox regulation of mitochondrial
proteins and proteomes by cysteine thiol switches. Mitochondrion; 33:72–83. PMID:
27456428. doi:10.1016/j.mito.2016.07.010.
Nikiforova, V.J., J. Kopka, V. Tolstikov, O. Fiehn, L. Hopkins, et al., 2005. Systems rebalancing of
metabolism in response to sulfur deprivation, as revealed by metabolome analysis of
Arabidopsis plants. Plant Physiol., 138: 304-318.
Nishikawa, T., D. Edelstein, and M. Brownlee, 2000. The missing link: A. single unifying mechanism
for diabetic complications. Kidney Int., 58 (Suppl):S26–S30. https://doi.org/10.1046/j.1523-
1755.2000.07705.x.
Niu Xiaomu, N.X., R.A. Bressan, P.M. Hasegawa, and J.M. Pardo, 1995. “Ion homeostasis in NaCl
stress environments,” Plant Physiology, 109(3):735–742,
Noji, M., K. Saito, 2007. Metabolic engineering of sulfur assimilation in plants. In: applications of plant
metabolic engineering. (ed.) Verpoorte R, A.lfermann AW, J.ohnson TS. Springer,
Netherlands, 297-309.
Noreen, Z., M. Ashraf, and N.A. Akram, 2010. Salt-induced modulation in some key gas exchange
characteristics and ionic relations in pea (Pisum sativum L). and their use as selection criteria.
Crop Pasture Sci. 61: 396–378. doi: 10.1071/CP09255.
Nounjana, N., P.T. Nghiab, and P. Theerakulpisuta, 2012. Exogenous proline and trehalose promote
recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and
expression of related genes. J. Plant Physiol., 169:596–604.
Nxele, X., A. Klein, and B.K. Ndimba, 2017. Drought and salinity stress alters ROS. accumulation,
water retention, and osmolyte content in sorghum plants. S. Afr. J. Bot., 108: 261–266.
[CrossRef]
Oates, P.J., 2002. Polyol pathway and diabetic peripheral neuropathy. Int. Rev. Neurobiol., 50:325–
392.
Oertli, J.J., 1968. Extracellular salt accumulation a possible mechanism of salt injury in plants.
Agrochimica, 12:461–469.
Oertli, J.J., 1991. Nutrient management under water and salinity stress. In: Proceeding of the
symposium on nutrient management for sustained productivity. Dept Soils Punjab Agric
UnverLudhiana, India, 138–165.
Ogawa, S., and S. Mitsuya 2012. S-methylmethionine is involved in the salinity tolerance of
Arabidopsis thaliana plants at germination and early growth stages. Physiol. Plant, 144: 13-19.
Oh, D.-H., S.Y. Lee, R.A. Bressan, D.-J. Yun, and H.J. Bohnert, 2010. “Intracellular consequences of
SOS1 deficiency during salt stress,” Journal of Experimental Botany, 61(4):1205–1213.
Ohnishi, N., and N. Murata, 2006. Glycine betaine counteracts the inhibitory effects of salt stress on
the degradation and synthesis of D1 proteinduring photoinhibition in Synechococcussp. PCC.
7942. Plant Physiol., 141:758–765
Omoto, E., M. Taniguchi, and H. Miyake, 2010. Effects of salinity stress on the structure of bundle
sheath and mesophyll chloroplasts in NAD-malic enzyme and PCK. type C4 plants. Plant Prod.
Sci. 13: 169–176. doi: 10.1626/pps.13.169.
Ortiz-Espín, A., R. Iglesias-Fernández, A. Calderón, P. Carbonero, F. Sevilla, and A. Jiménez, 2017.
Mitochondrial AtTrxo1 is transcriptionally regulated by AtbZIP9 and AtAZF2 and affects seed
germination under saline conditions. J. Exp Bot PMID: 28184497; 68:1025–1038.
doi:10.1093/jxb/erx012.

386
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Othman, Y., G. Al-Karaki, A.R. Al-Tawaha, and A. Al-Horani, 2006. Variation in germination and ion
uptake in barley genotypes under salinity conditions. World J. Agric., Sci 2:11–15.
Pang, Q., J. Guo, S. Chen, Y. Chen, L. Zhang, M. Fei, S. Jin, M. Li, Y. Wang, and X. Yan, 2012. Effect
of salt treatment on the glucosinolate-myrosinase system in Thellungiella salsuginea. Plant soil
355: 363-374.
Pang, Q., S. Chen, S. Dai, Y. Chen, Y.Wang, and X. Yan, 2010. “Comparative proteomics of salt
tolerance in Arabidopsis thaliana and Thellungiella halophila,” Journal of Proteome Research,
9(5):2584–2599.
Pang, Q., S. Chen, S. Dai, Y. Wang, Y. Chen, and X. Yan, 2010. Comparative proteomics of salt
tolerance in Arabidopsis thaliana and Thellungiella halophila. J. Proteome Res 9:2584–2599
Pannaga, K., R. Kosala, F. Rochus, H.S. Prakash, S. Lukas and M.K. Mathew, 2009. The role of root
apoplastic transport barriers in salt tolerance of rice (Oryza sativa L)., Plant a 2009. 230:119–
134 DOI. 10.1007/s00425-009-0930-6.
Paramo, L.A., A.A. Feregrino-P´erez, Guevara, R., Mendoza, S., and Esquivel, K., 2020. Nanoparticles
in agroindustry: applications, toxicity, challenges, and trends. Nanomaterials, 10: 1654.
Parida, A.K., A.B. Das, and B. Mittra, 2004. Effects of salt on growth, ion accumulation photosynthesis
and leaf anatomy of the mangrove, B.ruguiera parviflora. Trees-Struct Funct., 18:167–174.
Parida, A.K., A.B. Das, and P. Mohanty, 2004. “Investigations on the antioxidative defence responses
to NaCl stress in a mangrove, B.ruguiera parviflora: differential regulations of isoforms of some
antioxidative enzymes,” Plant Growth Regulation, 42(3):213–226.
Parida, A.K., and A.B. Das 2005. Salt tolerance and salinity effect on plants: a review. Ecotoxicol.
Environ., Saf., 60:324–349.
Parida, A.K., and A.B. Das, 2005. Salt tolerance and salinity effects on plants: A Review. Ecotoxicol.
Environ. Saf., 60: 324–349. [CrossRef] [PubMed].
Parihar, P., S. Samiksha, S. Rachana, P.S. Vijay and M.P. Sheo 2015. Effect of salinity stress on plants
and its tolerance strategies: a review, Environ Sci. Pollut. Res., 22:4056–4075 DOI.
10.1007/s11356-014-3739-1.
Parihar, P., S. Singh, R. Singh, V.P. Singh, and S.M. Prasad, 2015. Effect of salinity stress on plants
and its tolerance strategies: A Review. Environ. Sci. Pollut. Res., 22: 4056–4075. [CrossRef]
[PubMed].
Paz, R.C., H. Reinoso, F.D. Espasandin, F.A. González Antivilo, P.A. Sansberro, R.A. Rocco,
O.A.Ruiz, and A.B. Menendez, 2014. Akaline, saline and mixed saline–alkaline stresses induce
physiological and morpho-anatomical changes in Lotus tenuis shoots. Plant Biol., 16: 1042–
1049. [PubMed]
Peng, H., Z.hang, J., 2009. Plant genomic DNA. methylation in response to stresses: potential
applications and challenges in plant breeding. Prog. Nat. Sci., 19: 1037–1045.
Peng, Z., M.Wang, F. Li, H. Lv, C. Li, and G. Xia, 2009. Aproteomic study of the response to salinity
and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8:2676–2686
Per, T.S., N.A. Khan, A. Masood, and M. Fatma, 2016. Methyl jasmonate alleviates cadmium-induced
photosynthetic damages through increased S-assimilation and glutathione production in
mustard. Front. Plant Sci., 7, 1933. [CrossRef]
Per, T.S., N.A. Khan, P.S. Reddy, A. Masood, M. Hasanuzzaman, M.I.R. Khan, and N.A. Anjum, 2017.
Approaches in modulating proline metabolism in plants for salt and drought stress tolerance,
P.hytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem., 115:126–140.
[CrossRef]
Pereira, A.D.E.S., C.O. Halley, F.F. Leonardo and S. Catherine, 2021. Nanotechnology Potential in
Seed Priming for Sustainable Agriculture, Nanomaterials, 11: 267.
https://doi.org/10.3390/nano11020267 www.mdpi.com/journal/nanomaterials
Pérez-López, U., A. Robredo, M. Lacuesta, C. Sgherri, A. Mena-Petite, et al., 2010. Lipoic acid and
redox status in barley plants subjected to salinity and elevated CO2. Physiol Plant, 139: 256-
268.
Persak, H., and A. Pitzschke, 2013. Tight interconnection and multi-level control of Arabidopsis
MYB44 in MAPK. cascade signalling. PLoS. One 8:e57547.

387
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Perveen, S., M. Shahbaz, and M. Ashraf, 2010. Regulation in gas exchange and quantum yield of
photosystem II. (PSII) in salt-stressed and non-stressed wheat plants raised from seed treated
with triacontanol. Pakistan J. Bot. 42: 3073–3081.
Pinheiro, H.A., J.V. Silva, L. Endres, V.M. Ferreira, C.A. de Câmara, F.F. Cabral, et al., 2008. Leaf gas
exchange, chloroplastic pigments and dry matter accumulation in castor bean (Ricinus
communis L. seedlings subjected to salt stress conditions. Ind. Crops Prod. 27: 385–392. doi:
10.1016/j.indcrop.2007.10.003.
Piotr, S., and K. Grazyna, 2005. Antioxidant defense in the leaves of C3 and C4 plants under salinity
stress. Physiol Plant, 125:31–40.
Pitzschke, A., A. Djamei, F. Bitton, and H. Hirt, 2009. A. major role of the MEKK1-MKK1/2-MPK4
pathway in ROS. signalling. Mol. Plant, 2: 120–137.
Popova, L.P., Z.G. Stoinova, and L.T. Maslenkova, 1995. “Involvement of abscisic acid in
photosynthetic process in Hordeum vulgare L. during salinity stress,” Journal of Plant Growth
Regulation, 14(4):211–218.
Pravin V. Jadhav, P.rashant B. Kale, M.angesh P.M., C.G. Deepti, S.D. Mahendra, S.M. Shyam,
S.N. Ravindra, S.M. Shyamsundar, V. Philips, G.M. Joy and G.D. Raviprakash, 2018. Abiotic
Stress Tolerance Mechanisms in Plants, P.ages 1–84 Edited by: Gyanendra K. Rai,
R.anjeet Ranjan Kumar and Sreshti Bagati Copyright © Narendra Publishing House, Delhi,
India.
Prodhan, M.A., P.M. Finnegan, and H. Lambers, 2019. How does evolution in phosphorus-
impoverished landscapes impact plant nitrogen and sulfur assimilation? Trends Plant Sci. 24:
69–82. [CrossRef]
Pulido, P., R. Cazalis, F.J. Cejudo, and A. Ame, 2009. An antioxidant redox system in the nucleus of
wheat seed cells suffering oxidative stress. Plant J., 132–145. PMID: 18786001.
doi:10.1111/j.1365- 313X.2008.03675.x.
Qadir, M., and S. Schubert, 2002. Degradation processes and nutrient constraints in sodic soils. Land
Degrad. Dev., 13:275–294
Qiu, Q.S., Y. Guo, F.J. Quintero, J.M. Pardo, K.S. Schumaker, and J.K. Zhu, 2004. Regulation of
vacuolar Naþ/Hþ exchange in Arabidopsis thaliana by the salt-overly sensitive (SOS) pathway.
J. Biol. Chem., 279:207–215.
Quan, R., H. Lin, I. Mendoza, Y. Zhang, W.Cao, Y. Yang, M. Shang, S. Chen, J.M. Pardo, and Y. Guo,
2007. SCaBP8/CBL10, a putative calcium sensor, interacts with theprotein kinase SOS2 to
protect Arabidopsis shoots from salt stress. Plant Cell, 19:1415–1431.
Queval, G., D. Thominet, H. Vanacker, M. Miginiac-Maslow, and B. Gakière, et al., 2009. H2 O2 -
activated up-regulation of glutathione in Arabidopsis involves induction of genes encoding
enzymes involved in cysteine synthesis in the chloroplast. Mol. Plant, 2: 344-356.
Quintero, F.J., M. Ohta, H. Shi, J.-K. Zhu, and J.M. Pardo, 2002. “Reconstitution in yeast of the
Arabidopsis SOS. signaling pathway for Na+ homeostasis,” Proceedings of the National
Academy of Sciences of the United States of America, 99(13):9061–9066.
Qureshi, A.S., M. Qadir, N. Heydari, H. Turral and A. Javadi, 2007. A Review of management strategies
for salt-prone land and water resources in Iran. Colombo, S.ri Lanka: International Water
Management Institute. 30p. (IWMI) Working Paper 125.
Rahman, S., H. Miyake, and Y. Takeoka, 2002. “Effects of exogenous glycinebetaine on growth and
ultrastructure of salt-stressed rice seedlings (Oryza sativa L).,” Plant Production Science,
5(1):33–44,
Rahman, S.U., W. Xiaojie, S. Muhammad, B. Owais, L. Yanliang, and C. Hefa, 2022. A Review of the
influence of nanoparticles on the physiological and biochemical attributes of plants with a focus
on the absorption and translocation of toxic trace elements, E.nvironmental Pollution 310
119916
Rahnama, A., R.A. James, K. Poustini, and R. Munns, 2010. “Stomatal conductance as a screen for
osmotic stress tolerance in durum wheat growing in saline soil,” Functional Plant Biology,
37(3):255–263.
Rais, L., A. Masood, A. Inam, and N. Khan, 2013. Sulfur and nitrogen co-ordinately improve
photosynthetic efficiency, growth and proline accumulation in two cultivars of mustard under
salt stress. J. Plant Biochem. Physiol., 1. [CrossRef]

388
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Rambla, J.L., F. Vera-Sirera, M.A. Bl´azquez, J. Carbonell, and A. Granell, 2010. “Quantitation of
biogenic tetraamines in Arabidopsis thaliana,” Analytical Biochemistry, 397(2):208–211,
Rania M.A.N., A.K. Hedaya, E.G. Ahmed, J.A. Juan, S. Agnieszka, U. Christian and T.A. Magdi, 2020
. Physiological and a natomical Mechanisms in Wheat to Cope with Salt Stress Induced by
Seawater, Plant s, 9, 237; doi: 10.3390/plants9020237 www.mdpi.com/journal/plants
Rapala-Kozik, M., E. Kowalska, and K. Ostrowska, 2008. Modulation of thiamine metabolism in Zea
mays seedlings under conditions of abiotic stress. J. Exp. Bot., 59: 4133-4143.
Rapala-Kozik, M., N. Wolak, A.K. Kujda and M. Banas, 2012. The upregulation of thiamine (vitamin
B1. biosynthesis in Arabidopsis thaliana seedlings under salt and osmotic stress conditions is
mediated by abscisic acid at the early stages of this stress response. BMC. Plant Biol., 12: 1-
21.
Rasheed, F., A.A. Naser, M. Asim, S. Adriano, and A.K. Nafees, 2020. The key roles of salicylic acid
and sulfur in plant salinity stress tolerance, Journal of Plant Growth Regulation
https://doi.org/10.1007/s00344-020-10257-3.
Rasoulnia, A., M.R. Bihamta, S.A. Peyghambari, H. Alizadeh, and A. Rahnama, 2011. Proteomic
response of barley leaves to salinity. Mol. Biol. Rep., 38:5055–5063.
Rastogi, A., M. Zivcak, O. Sytar, H.M. Kalaji, X. He, S. Mbarki, and M. Brestic, 2017. Impact of metal
and metal oxide nanoparticles on plant: a critical review. Front Chem., 5:78.
https://doi.org/10.3389/ fchem.2017.00078.
Rawia Eid, A., L.S. Taha, and S.M.M. Ibrahiem, 2011. “Alleviation of adverse effects of salinity on
growth, and chemical constituents of marigold plants by using glutathione and ascorbate,”
Journal of Applied Sciences Research, 7:714–721.
Raza, S.H., H.U.R. Athar, and M. Ashraf, 2006. Influence of exogenously applied glycinebetaine on
the photosynthetic capacity of two differently adapted wheat cultivars under salt stress. Pakistan
J. Bot. 38: 341–351.
Reddy, M.P., S. Sanish, and E.R.R. Iyengar, 1992. “Photosynthetic studies and compartmentation of
ions in different tissues of Salicornia brachiata Roxb. under saline conditions,” Photosynthetica,
26:173–179.
Reichheld, J.P., C. Riondet, V. Delorme, F. Vignols, and Y. Meyer, 2010. Thioredoxins and
glutaredoxins in development. Plant Sci., 178:420–423. doi:10.1016/j.plantsci.2010.03.001.
Reichheld, J.P., E. Meyer, M. Khafif, G. Bonnard, and Y. Meyer, 2005. AtNTRB. is the major
mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS. Lett., 579:337–342.
doi:10.1016/j. febslet.2004.11.094.
Renberg, L., A.I. Johansson, T. Shutova, H. Stenlund, A. Aksmann, J.A. Raven, P. Gardeström, T.
Moritz, and G. Samuelsson, 2010. A. metabolomic approach to study major metabolite changes
during acclimation to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiol., 154: 187–
196.
Rico, C.M., M.I. Morales, R. McCreary, H. Castillo-Michel, A.C. Barrios, J. Hong, A. Tafoy, W.Y.
Lee, A. Varela-Ramirez, J.R. Peralta-Videa, and J.L. Gardea-Torresdey, 2013. Cerium oxide
nanoparticles modify the antioxidative stress enzyme activities and macromolecule
composition in rice seedlings. Environ. Sci. Technol., 47(24):14110–14118.
https://doi.org/10.1021/es4033887
Riffat, A.L.I.A., M. Sajid, and A. Ahmad, 2020. Alleviation of adverse effects of salt stress on growth
og maize Zea mays L. by sulfur supplementation. Pak. J. Bot., 523: 763–773.
Rocha, F., E.L.-B. Manuel, P. Paulo and M.-R. Miriam, 2020. Cyanobacteria as a Nature-Based
Biotechnological Tool for Restoring Salt-Affected Soils, A.gronomy 10, 1321;
doi:10.3390/agronomy10091321 www.mdpi.com/journal/agronomy
Rodriguez, M.C., M. Petersen, and J. Mundy, 2010. Mitogen-activated protein kinase signaling in
plants. Annu. Rev. Plant Biol., 61:621–649.
Rogers, M.E., C.M. Grieve, and M.C. Shannon, 2003. Plant growth and ion relations in lucerne
(Medicagosativa L). in response to the combined effects of NaCl and P. Plant Soil, 253:187–
194.
Romero, L., A. Belakbir, L. Ragala, and J. M. Ruiz, 1997. Response of plant yield and leaf pigments to
saline conditions: effectiveness of different rootstocks in melon plants (Cucumis melo L). Soil
Sci. Plant Nutr. 43, 855–862. doi: 10.1080/00380768.1997.10414652

389
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Romero, L.C., J.R. Domínguez-Solis, G. Gutierrez-Alcala, and C. Gotor, 2001. Salt regulation of O-
acetylserine(thiollyase in Arabidopsis thaliana and increased tolerance in yeast. Plant Physiol
Biochem., 39: 643-647.
Romero-Aranda, M.R., O. Jurado, and J. Cuartero, 2006. Silicon alleviates the deleterious salt Effect
on tomato plant growth by improving plant water status. J. Plant Physiol., 163: 847–855.
[CrossRef] [PubMed].
Romero-Aranda, R., T. Soria, and S. Cuartero, 2001. Tomato plant-water uptake and plant-water
relationships under saline growth conditions. Plant Sci., 160:265–272.
Rossi, L., W. Zhang, L. Lombardini, and X. Ma, 2016. The impact of cerium oxide nanoparticles on
the salt stress responses of Brassica napus L. Environ. Pollut., 219:28–36.
Roxas, V.P., S.A. Lodhi, D.K. Garrett, J.R. Mahan, and R.D. Allen, 2000. Stress tolerance in transgenic
tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell.
Physiol., 41: 1229–1234. [CrossRef]
Roy, M. and R. Wu, 2002. “Overexpression of S-adenosylmethionine decarboxylase gene in rice
increases polyamine level and enhances sodium chloride-stress tolerance,” Plant Science,
163(5):987–992.
Roy, M. and R. Wu, 2002. Overexpression of S-adenosylmethionine decarboxylase gene in rice
increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci., 163: 987-
992.
Roy, M., and R. Wu, 2001. Arginine decarboxylase transgene expression and analysis of environmental
stress tolerance in transgenic rice. Plant Sci., 160: 869-875.
Roy, S.J., S. Negr˜ao, and M. Tester, 2014. “Salt resistant crop plants,” Current Opinion in
Biotechnology, 26:115–124.
Rozeff, N., 1995. Sugarcane and salinity—a review paper. Sugarcane, 5:8–19.
Rozema, J. and T. Flowers, 2008. “Ecology: crops for a salinized world,” Science, 322(5907):1478–
1480.
Ruiz, J.M., and E. Blumwald 2002. Salinity-induced glutathione synthesis in Brassica napus. Planta,
214: 965-969.
Sabaghnia, N., and M. Janmohammadi, 2014. Effect of nano-silicon particles application on salinity
tolerance in early growth of some lentil genotypes. Ann UMCS. Biol., 69:39–55.
Sabir, P., M. Ashraf, M. Hussain, and A. Jamil, 2009. Relationship of photosynthetic pigments and
water relations with salt tolerance of proso millet (Panicum Miliaceum L). accessions. Pakistan
J. Bot., 41: 2957–2964.
Sachdev, S. and S. Ahmad, 2021. Role of Nanomaterials in Regulating Oxidative Stress in Plants
Springer Nature Switzerland AG. 2021 J. M. Al-Khayri et al., (eds), N.anobiotechnology,
https://doi.org/10.1007/978-3-030-73606-4_13.
Sadak, S.h., A.A. Abd El-Monem, H.M.S. El-Bassiouny and Nadia M. Badr, 2012. Physiological
response of sunflower (Helianthus annuus L). to exogenous arginine and putrescine treatments
under salinity Stress. Journal of Applied Sciences Research, 8(10): 4943-4957.
Sade, N., M. Gebretsadik, R. Seligmann, A. Schwartz, R. Wallach, and M. Moshelion, 2010. The role
of tobacco aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield
production under salt stress. Plant Physiol. 152, 245–254. doi: 10.1104/pp.109.145854.
Sah, S.K., K.R. Reddy, and J. Li, 2016. Abscisic acid and abiotic stress tolerance in crop plants. Front.
Plant Sci., 7, 571. [CrossRef].
Saha, P., P. Chatterjee, and A.K. Biswas, 2010. NaCl pretreatment alleviates salt stress by enhancement
of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiata
L.Wilczek. Indian J. Exp. Biol., 48:593–600.
Sairam, R.K. and A. Tyagi, 2004. “Physiology and molecular biology of salinity stress tolerance in
plants,” Current Science, 86(3):407–421
Sairam, R.K., and A. Tyagi, 2004. Physiology and molecular biology of salinity stress tolerance in
plants. Curr. Sci., 86: 407-412.
Sairam, R.K., K.V. Roa, and G.C. Srivastava, 2002. Differential response of wheat genotypes to long
term salinity stress in relation to oxidative stress, antioxidant activity and osmolyte
concentration. Plant Sci., 163:1037–1046.

390
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Sakamoto, A., and M.N. Alia, 1998. Metabolic engineering of rice leading to biosynthesis of glycine
betaine and tolerance to salt and cold. Plant Mol. Biol., 38:1011–1019.
Salim, B., A. Abou El-Yazied, Y. Salama, A. Raza, and H.S. Osman, 2021. Impact of silicon foliar
application in enhancing antioxidants, growth, flowering and yield of squash plants under
deficit irrigation condition. Ann. Agricult. Sci. 66: 176–183.
Samajova, O., O. Plihal, M. Al-Yousif, H. Hirt, and J. Samaj, 2013. Improvement of stress tolerance in
plants by genetic manipulation of mitogen activated protein kinases. Biotechnol. Adv., 31:118–
128.
Sánchez-Aguayo, I., J.M. RodrÃguez-Galán, R. GarcÃa, J. Torreblanca, and J.M. Pardo, 2004. Salt
stress enhances xylem development and expression of S-adenosylL-methionine synthase in
lignifying tissues of tomato plants. Planta, 220: 278- 285.
Sanders, D., 2000. “Plant biology: the salty tale of Arabidopsis,” Current Biology, 10(13):R486–R488,
Santos, C.V., 2004. Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower
leaves. Sci. Hortic. 103, 93–99. doi: 10.1016/j.scienta.2004.04.009.
Santos, M.R.D., M.A. Martinez, S.L.R. Donato, and E.F. Coelho, 2014. ’Tommy Atkins’ mango yield
and photosynthesis under water deficit in semiarid region of Bahia. Rev. Brasil. Engenharia
Agrícola Ambiental, 18:899–907.
Sattar, A., M.A. Cheema, T. Abbas, A. Sher, M. Ijaz, and M. Hussain, 2017. Separate and combined
effects of silicon and selenium on salt tolerance of wheat plants. Russ. J. Plant Physl., 64: 341–
348. [CrossRef]
Sauter, M., B. Moffatt, M.C. Saechao, R. Hell, and M. Wirtz, 2013. Methionine salvage and S-
adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.
Biochem J., 451: 145-154.
Sawada, H., I.-S. Shim, and K. Usui, 2006. “Induction of benzoic acid 2-hydroxylase and salicylic acid
biosynthesis-Modulation by salt stress in rice seedlings,” Plant Science, 171(2): 263– 270.
Saxena, S.C., H. Kaur, P. Verma et al., 2013. “Osmoprotectants: potential for crop improvement under
adverse conditions,” in PlantAcclimation to Environmental Stress):197–232, S.pringer, New
York, N.Y., USA.
Schmidtmann, E., A.-C. König, A. Orwat, D. Leister, M. Hartl, and I. Finkemeier, 2014. Redox
regulation of Arabidopsis mitochondrial citrate synthase. Mol Plant; 7:156–169. PMID:
24198232. doi:10.1093/mp/sst144.
Schroeder, J.I., E. Delhaize, W.B. Frommer et al., 2013. “Using membrane transporters to improve
crops for sustainable food production,” Nature, 497:60–66.
Schurmann, P., and J.P. Jacquot, 2000. Plant thioredoxin systems revisited. Annu Rev Plant Physiol
Plant Mol. Biol., 51: 371-400.
Schwarzländer, M., M.D. Fricker, C. Müller, L. Marty, T. Brach, J. Novak, L.J. Sweetlove, R.Hell, and
A.J. Meyer, 2008. Confocal imaging of glutathione redox potential in living plant cells. J.
Microsc., 231: 299–316. [CrossRef] [PubMed]
Schweighofer, A., V. Kazanaviciute, E. Scheikl, M. Teige, R. Doczi, H. Hirt, M. Schwanninger, M.
Kant, R. Schuurink, F. Mauch, A. Buchala, F. Cardinale, and I. Meskienea, 2007. The PP2C-
type phosphatase AP2C1, which negatively regulates MPK4and MPK6, modulates seedlings.
Plant Sci., 175:631–641.
Seemann, J.R., and C. Critchley, 1985. Effects of salt stress on the growth, ion contents, stomatal
behaviour and photosynthetic capacity of a salt sensitive species, P.haseolus vulgaris L. Planta,
164:66–69.
Sehar, Z., A. Masood, and N.A. Khan, 2019. Nitric oxide reverses glucose-mediated photosynthetic
repression in wheat (Triticum aestivum L). under salt stress. Environ. Exp. Bot., 161: 277–289.
[CrossRef]
Semida, W.M., R.S. Taha, M.T. Abdelhamid, and M.M. Rady, 2014. Foliar-applied α-tocopherol
enhances salt-tolerance in Vicia faba L. plants grown under saline conditions. S. Afr. J. Bot.,
95: 24–31. [CrossRef]
Semiz, G.D., A. Ünlukara, E. Yurtseven, D.L. Suarez, and I. Telci, 2012. Salinity impact on yield, water
use,mineral and essential oil contentof fennel (Foeniculum vulgare MilL). J. Agric Sci.,
18:177–186.

391
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Sengupta, S., and A.L. Majumder, 2009. Insight into the salt tolerance factors of a wild halophytic rice
Porteresia coarctata: a physiological and proteomic approach. Planta, 229:911–929.
Serrato, A.J., and F.J. Cejudo, 2003. Type-h thioredoxins accumulate in the nucleus of developing
wheat seed tissues suffering oxidative stress. Planta; 217:392–399. PMID: 14520565. Doi:
10.1007/ s00425-003-1009-4.
Serrato, A.J., J.M. Pérez-Ruiz, M.C. Spínola, and F.J. Cejudo 2004. A. novel NADPH. thioredoxin
reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress
in Arabidopsis thaliana. J. Biol. Chem., 279: 43821-43827.
Seth, C.S., T. Remans, E. Keunen, M. Jozefczak, H. Gielen, K. Opdenakker, and A. Cuypers, 2012.
Phytoextraction of toxic metals: A. central role for glutathione. Plant Cell Environ. 35: 334–
346. [CrossRef]
Sewelam, N., K. Kazan, and P.M. Schenk, 2016Global plant stress signaling: Reactive oxygen species
at the cross-road. Front. Plant Sci., 7, 187. [CrossRef]
Shabala, S., O. Babourina, and I. Newman, 2000. Ion-Specific Mechanisms of Osmoregulation in Bean
Mesophyll Cells. Journal of Experimental Botany, 51: 1243-1253.
https://doi.org/10.1093/jexbot/51.348.1243
Shalata, A., V. Mittova, M. Volokita, M. Guy, and M. Tal, 2001. Response of the cultivated tomato and
its wild salt-tolerant relative Lycopersicon pennellii to salt-dependent oxidative stress: The root
antioxidative system. Physiol Plant, 112: 487-494.
Shanker, A.K., and B. Venkateswarlu 2011. Abiotic stress in plants—mechanisms and adaptations. In:
TechJaneza Trdine 9, 51000 Rijeka, Croatia.
Sharma, A., V. Kumar, B. Shahzad, M. Ramakrishnan, G.P. Singh Sidhu, A.S. Bali, et al., 2020.
Photosynthetic response of plants under different abiotic stresses: a review. J. Plant Growth
Regul. 39: 509–531. doi: 10.1007/s00344-019-10018-x
Shevyakova, N.I., L.I. Musatenko, L.A. Stetsenko, et al., 2013. “Effects of abscisic acid on the contents
of polyamines and proline in common bean plants under salt stress,” Russian Journal of Plant
Physiology, 60:200–211.
Shi, H., and J.K. Zhu, 2002. SOS4, a pyridoxal kinase gene, is required for root hair development in
Arabidopsis. Plant Physiol., 129:585–593.
Shi, H., F.J. Quintero, J.M. Pardo, and J.-K. Zhu, 2002. “The putative plasma membrane Na+/H+
antiporter SOS1 controls longdistance Na+ transport in plants,” Plant Cell, 14(2):465–477.
Shi, H., M. Ishitani, C. Kim, and J.-K. Zhu, 2000. “The Arabidopsis thaliana salt tolerance gene SOS1
encodes a putative Na+/H+ antiporter,” Proceedings of the National Academy of Sciences of
the United States of America, 97(12): 6896–6901.
Shi, H., M. Ishitani, C. Kim, and J.K. Zhu, 2000. The Arabidopsis thaliana salt tolerance gene SOS1
encodes a putative Na+/H+ antiporter. Proc. Natl. Acad. Sci. USA. 97:6896–6901.
Shi, Y., Y. Wang, T.J. Flowers, and H. Gong, 2013. “Silicon decreases chloride transport in rice (Oryza
sativa L). in saline conditions,” Journal of Plant Physiology, 170(9):847–853.
Shi, Y., Y. Zhang, H. Yao, J. Wu, H. Sun, and H. Gong, 2014Silicon improves seed germination and
alleviates oxidative stress of bud seedlings in tomato under water deficit stress. Plant Physiol.
Biochem., 78: 27–36. [CrossRef]
Shrivastava, P., and R. Kumar, 2014. Soil salinity: a serious environmental issue and plant growth
promoting bacteria as one of the tools for its alleviation. Saudi Journal of Biological Science,
22: 123–131.
Shu, S., S.R. Guo, and L.Y. Yuan, 2012. “A Review: polyamines and photosynthesis,” in Advances in
Photosynthesis—Fundamental Aspects, M. M. Najafpour, (E.d.)439–464, I.nTech, R.ijeka,
Croatia.
Shulaev, V., D. Cortes, G. Miller, and R. Mittler 2008. Metabolomics for plant stress response. Physiol
Plant, 132:199–208.
Siddiqui, H., K.B.M. Ahmed, F. Sami, and S. Hayat, 2020. Silicon nanoparticles and plants: current
knowledge and future perspectives. Sustain. Agric. Rev., 41: 129–142.
Siddiqui, M.H., and M.H. Al-Whaibi, 2014. Role of nano-SiO2 in germination of tomato
(Lycopersicum esculentum seeds milL). Saudi J. Biol. Sci., 21:13–17.
Siddiqui, M.H., M.H. Al-Whaibi, M. Faisal, and A.A. Al Sahli, 2014. Nano-silicon dioxide mitigates
the adverse effects of salt stress on Cucurbita pepo L. Environ. Toxicol. Chem., 33:2429–2437.

392
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Silberbush, M., J. Ben-Asher, and J.E. Ephrath, 2005. A. model for nutrient and water flow and their
uptake by plants grown in a soilless culture. Plant Soil, 271(1-2):309–319.
Singh, A., I. Hussain, N.B. Singh, and H. Singh, 2019. Uptake, translocation and impact of green
synthesized nanoceria on growth and antioxidant enzymes activity of Solanum lycopersicum
L. Ecotoxicol. Environ. Saf. 182, 109410.
Singh, M., V.P. Singh, and S.M. Prasad, 2016. Responses of photosynthesis, nitrogen and proline
metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen
supplementation. Plant Physiol. Biochem., 109: 72–83. [CrossRef]
Singh, S., V.P. Singh, S.M. Prasad, S. Sharma, N. Ramawat, and N.K. Dubey, 2019. Interactive effect
of silicon (Si. and salicylic acid (SA) in maize seedlings and their mechanisms of cadmium (Cd.
toxicity alleviation. J. Plant Growth Regul. 38: 1587–1597.
Singha, R.K., S. Debanjana, S. Milan, N.M. Udit, C. Jyoti, P.B. Laxmi, L. Devidutta, C. Subhash, K.
Vivek, D.I. Prajjal, P. Saurabh, V. Pavla, G. Aayushi, B. Marian and E. Ayman, 2021. Crucial
Cell Signaling Compounds Crosstalk and Integrative Multi-Omics Techniques for Salinity
Stress Tolerance in Plants, F.rontiers in Plant Science, www.frontiersin.org, 12: 670369.
Singla-Pareek, S.L., M.K. Reddy and S.K. Sopory, 2003. Genetic engineering of the glyoxalase
pathway in tobacco leads to enhanced salinity tolerance, P.NAS. December 9, 100 (25) 14673.
Snapp, S.S., C. Shennan, and A.V. Bruggen 1991. Effects of salinity on severity of infection by
Phytophthora parasitica Dast., ion concentrations and growth of tomato, L.ycopersicon
esculentum Mill. New Phytologist, 119: 275–284.
Sobhanian, H., N. Motamed, F.R. Jazii, T. Nakamura, and S. Komatsu, 2010a. Salt stress induced
differential proteome and metabolome response in the shoots of Aeluropus lagopoides
(Poaceae., a halophyte C4 plant. J. Proteome Res., 9:2882–2897.
Sobhanian, H., R. Razavizadeh, Y. Nanjo, A.A. Ehsanpour, F.R. Jazii, N. Motamed, and S. Komatsu,
2010b. Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome
Sci., 8:19.
Sofy, M.R., K.M. Elhindi, S. Farouk, and M.A. Alotaibi, 2020. Zinc and paclobutrazol mediated
regulation of growth, upregulating antioxidant aptitude and plant productivity of pea plants
under salinity. Plants, 9: 1197.
Solani, D.M., 2018. Biochemical changes in diabetic retinopathy triggered by Hyperglycaemia: A
Review. African Vision and Eye Health ISSN: (Online) 2410-1516, (Print) 2413-3183.
Soliman, A.S., S.A. El-feky, and E. Darwish, 2015. Alleviation of salt stress on Moringa peregrina
using foliar application of nanofertilizers. J. Hortic. For., 7(2):36–47.
Soundararajan, P., I. Sivanesan, S. Jana, and B.R. Jeong, 2014. “Influence of silicon supplementation
on the growth and tolerance to high temperature in Salvia splendens,” Horticulture,
E.nvironment, and Biotechnology, 55(4):271–279.
Soylemezoglu, G., K. Demir, A. Inal, and A. Gunes, 2009. Effect of silicon on antioxidant and stomatal
response of two grapevine (Vitis vinifera L). rootstocks grown in boron toxic, saline and boron
toxic-saline soil. Sci. Hortic.-Amsterdam, 123: 240–246. [CrossRef]
Stevens, F.J., A.D. Li, S.S. Lateef, and L.E. Anderson, 1997. Identification of potential inter-domain
disulfides in three higher plant mitochondrial citrate synthases: paradoxical differences in
redox-sensitivity as compared with the animal enzyme. Photosyn Res., 185–197.
doi:10.1023/A:1005991423503.
Sugimoto, M., and K. Takeda, 2009. Proteomic analysis of specific proteins in the root of salt-tolerant
barley. Biosci. Biotechnol. Biochem., 73:2762– 2765.
Sun, C., Z. Yuxue, L. Lijuan, L. Xiaoxia, L. Baohai, J. Chongwei and L. Xianyong, 2021. Molecular
functions of nitric oxide and its potential applications in horticultural crops
https://doi.org/10.1038/s41438-021-00500-7.
Sundby, C., and B. Andersson, 1985. Temperature-induced reversible migration along the thylakoid
membrane of photosystem II. regulates it association with LHC-II. FEBS. Lett. 191: 24–28.
doi: 10.1016/0014-5793(85) 80986-8
Sung, C.H. and J.K. Hong, 2010. “Sodium nitroprusside mediates seedling development and attenuation
of oxidative stresses in Chinese cabbage,” Plant Biotechnology Reports, 4(4):243–251,
Sunkar, R., and J.K. Zhu 2004. Novel and stress-regulated microRNAs and other small RNAs from
Arabidopsis. Plant Cell, 16:2001–2019.

393
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Szabolcs, I. 1974. Salt affected soils in Europe. Martinus Nijhoff, The Hague, 63.
Sze, H., X. Li, and M.G. Palmgren, 1999. Energization of plant membranes by Hþ-pumping ATPases:
regulation and biosynthesis. Plant Cell, 11: 677–689.
Tada, Y., and T. Kashimura, 2009. Proteomic analysis of salt-responsive proteins in the mangrove plant,
B.ruguiera gymnorhiza. Plant Cell Physiol., 50:439–446.
Taffouo, V.D., O.F. Wamba, E. Youmbi, G.V. Nono, and A. Akoa, 2010. Growth, yield, water status
and ionic distribution response of three Bambara groundnut (Vigna subterranea L). verdc.
landraces grown under saline conditions. Int. J. Bot. 6: 53–58. doi: 10.3923/ijb.2010.53.58.
Tahir, M.A., T. Aziz, M. Farooq, and G. Sarwar, 2012. “Siliconinduced changes in growth, ionic
composition, water relations, chlorophyll contents and membrane permeability in two
saltstressed wheat genotypes,” Archives of Agronomy and Soil Science, 58(3):247–256.
Taji, T., M. Seki, M. Satou, T. Sakurai, M. Kobayashi, K. Ishiyama, Y. Narusaka, M. Narusaka, J.K.
Zhu, and K. Shinozaki, 2004. Comparative genomics in salt tolerance between Arabidopsis and
Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol., 35:
1697–1709.
Takahashi T. and J.-I. Kakehi, 2010. “Polyamines: ubiquitous polycations with unique roles in growth
and stress responses,” Annals of Botany, 105(1):1–6.
Takahashi, E., J.F. Ma and Y. Miyake, 1990. The possibility of silicon as an essential element for higher
plants. Comm. Agric. Food Chem., 2: 99-122.
Takahashi, H., S. Kopriva, M. Giordano, K. Saito, and R. Hell, 2011. Sulfur assimilation in
photosynthetic organisms: molecular functions and regulations of transporters and assimilatory
enzymes. Annu. Rev. Plant Biol., 62: 157-184.
Tang, X., X. Mu, H. Shao, H. Wang, and M. Brestic, 2015. Global plant-responding mechanisms to salt
stress: physiological and molecular levels and implications in biotechnology. Crit. Rev.
Biotechnol., 35(4):425–437. https://doi.org/10.3109/07388551.2014.889080
Tarchoune, I., C. Sgherri, O. Baâtour, R. Izzo, M. Lachaal, et al., 2013. Effects of oxidative stress
caused by NaCl or Na2 SO4 excess on lipoic acid and tocopherols in Genovese and Fine basil
(Ocimum basilicum) Ann. Applied Bio., 163: 23-32.
Tarczynski, M.C., R.G. Jensen, and H.J. Bohnert 1993. Stress protection of transgenic plants by
production of the osmolyte mannitol. Science, 259:508–510.
Tavakkoli, E., F. Fatehi, S. Coventry, P. Rengasamy, and G.K. McDonald, 2011. Additive effects of
Na+ and Cl− ions on barley growth under salinity stress. J. Exp. Bot., 62:2189–2203.
Tayefi-Nasrabadi, H., G. Dehghan, B. Daeihassani, A. Movafegi, and A. Samadi, 2011. Some
biochemical properties of guaiacol peroxidases as modified by salt stress in leaves of salt-
tolerant and salt-sensitive safflower (Carthamus tinctorius L.cv) cultivars. African J.
Biotechnol. 10:751–763. doi: 10.5897/ AJB10.1465.
Thakur, P., S. Kumar, J.A. Malik, J.D. Berger, and H. Nayyar, 2010. Cold stress effects on reproductive
development in grain crops: an overview. Environ. Exp. Bot., 67:429–443.
Thomas, C.R., S. George, A.M. Horst, Z.X. Ji, R.J. Miller, J.R. Peralta-Videa, T.A. Xia, S. Pokhrel, L.
Madler and J.L. Gardea-Torresdey, 2011. Nanomaterials in the environment: from materials to
high-through put screening to organisms. ACS. Nano 5:13–20.
Thomas, J.C., M. Sepahi, B. Arendall, and H.J. Bohnert, 1995. “Enhancement of seed germination in
high salinity by engineeringmannitol expression in Arabidopsis thaliana,” Plant, C.ell and
Environment, 18(7):801–806.
Thormählen I, T. Meitzel, J. Groysman, A.B. Öchsner, E. von Roepenack-Lahaye, B. Naranjo, F.J.
Cejudo, and P. Geigenberger, 2015. Thioredoxin f1 and NADPH-dependent thioredoxin
reductase C. have overlapping functions in regulating photosynthetic metabolism and plant
growth in response to varying light conditions. Plant Physiol., 169:1766–1786. PMID:
26338951. Doi:10.1104/ pp.15.01122.
Thorne, S.J., E.H. Susan and J.M.M. Frans, 2020. Is Silicon a Panacea for Alleviating Drought and Salt
Stress in Crops. Frontiers in Plant Science | www.frontiersin.org, A.ugust, 11:1221.
Tian, X., M. He, Z. Wang, J. Zhang, Y. Song, Z. He, and Y. Dong, 2015. Application of nitric oxide
and calcium nitrate enhances tolerance of wheat seedlings to salt stress. Plant Growth Regul.,
77: 343–356. [CrossRef]

394
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Tisi, A., R. Angelini, and A. Cona, 2008. “Wound healing in plants: cooperation of copper amine
oxidase and flavin-containing polyamine oxidase,” Plant Signaling and Behavior, 3(3):204–
206.
Tolaymat, T., A. Genaidy, W. Abdelraheem, D. Dionysiou, and C. Andersen, 2017. The effects of
metallic engineered nanoparticles upon plant systems: an analytic examination of scientific
evidence. Sci. Total Environ., 579: 93–106.
Tortella, G.R., O. Rubilar, N. Dur´an, M.C. Diez, M. Martínez, J. Parada, and A.B. Seabra, 2020. Silver
nanoparticles: toxicity in model organisms as an overview of its hazard for human health and
the environment. J. Hazard. Mater., 390: 121974.
Traverso, J.A., C. Micalella, A. Martinez, S.C. Brown, B. Satiat-Jeunema ître, T. Meinnel, and C.
Giglione, 2013. Roles of N-terminal fatty acid acylations in membrane compartment
partitioning: Arabidopsis h-Type thioredoxins as a case study. Plant Cell, 25:1056– 1077.
PMID: 23543785. doi:10.1105/tpc.112.106849.
Tripathi, D.K., K. Vishwakarma, V.P. Singh, V. Prakash, S. Sharma, S. Muneer, M. Nikolic,
R.Deshmukh, M. Vaculík, and F.J. Corpas, 2020b. Silicon crosstalk with reactive oxygen
species, phytohormones and other signaling molecules. J. Hazard. Mater., 124820.
Tripathi, D.K., P. Rai, G. Guerriero, S. Sharma, F.J. Corpas, and V.P. Singh, 2020a. Silicon induces
adventitious root formation in rice (Oryza sativa L). under arsenate stress with the involvement
of nitric oxide and indole-3-acetic acid. J. Exp. Bot.
Tripathi, D.K., S. Singh, V.P. Singh, S.M. Prasad, N.K. Dubey, and D.K. Chauhan, 2018. Silicon
nanoparticles more effectively alleviated UV-B. stress than silicon in wheat (Triticum aestivum.
seedlings. Plant Physiol. Biochem., 110: 70–81.
Tripathi, D.K., S.hweta, S. Singh, S. Singh, R. Pandey, V.P. Singh, N.C. Sharma, S.M. Prasad,
N.K.Dubey, and D.K. Chauhan, 2017a. An overview on manufactured nanoparticles in plants:
Uptake, translocation, accumulation and phytotoxicity. Plant Physiol. Biochem., 110: 2–12.
Tripathi, D.K., V.P. Singh, P. Ahmad, D.K. Chauhan, and S.M. Prasad, 2016. Silicon in plants:
advances and future prospects. Florida, F.L: CRC. Press.
Tuna, A.L., C. Kaya, D. Higgs, B. Murillo-Amador, S. Aydemir, and A.R. Girgin, 2008Silicon
improves salinity tolerance in wheat plants. Environ. Exp. Bot., 62: 10–16. [CrossRef]
Tuna, L.A., C. Kaya, M. Ashraf, H. Altunlu, I. Yokas, and B. Yagmur 2007. The effects of calcium
sulphate on growth, membrane stability and nutrient uptake of tomato plants grown under salt
stress. Environ. Exp. Bot., 59:173–178.
Tunc-Ozdemir, M., G. Miller, L. Song, J. Kim, A. Sodek, et al., 2009. Thiamin confers enhanced
tolerance to oxidative stress in Arabidopsis. Plant Physiol., 151: 421-432.
Tutej, N., M. Tarique, and R. Tutej, 2014. Rice SUV3 is a bidirectional helicase that binds both DNA.
and RNA. BMC. Plant Biol. 14:283. doi: 10.1186/s12870-014-0283-6
Tuteja, N., R.K. Sahoo, B. Garg, and R. Tuteja, 2013. “OsSUV3 dual helicase functions in salinity
stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa
L. cv.) IR64.,” The Plant Journal, 76(1):115–127.
Ulfat, M., H. Athar, M. Ashraf, N.A. Akram, and A. Jamil 2007. Appraisal of physiological and
biochemical selection criteria for evaluation of salt tolerance in canola (Brassica napus L). Pak.
J. Bot., 39:1593– 1608s
Urano, K., Y. Kurihara, M. Seki, and K. Shinozaki 2010. ‘Omics’ analyses of regulatory networks in
plant abiotic stress responses. Curr. Opin. Plant Biol., 13:132–138.
Urano, K., Y. Yoshiba, T. Nanjo et al., 2003. “Characterization of Arabidopsis genes involved in
biosynthesis of polyamines in abiotic stress responses and developmental stages,” Plant, C.ell
and Environment, 26(11):1917–1926.
Urano, K., Y. Yoshiba, T. Nanjo, T. Ito, K. Yamaguchi-Shinozaki, and K. Shinozaki, 2004.Arabidopsis
stress-inducible gene for arginine decarboxylase AtADC2 is required for accumulation of
putrescine in salt tolerance,” Biochemical and Biophysical Research Communications,
313(2):369–375.
Vaidyanathan, H., P. Sivakumar, R. Chakrabarty, and G. Thomas 2003. Scavenging of reactive oxygen
species in NaCl stressed rice (Oryza sativa L). differential response in salttolerant and sensitive
varieties. Plant Sci., 165: 1411-1418.

395
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Van der Werf, A., A. Kooijman, R. Welschen, and H. Lambers, 1988. Respiratory energy costs for the
maintenance of biomass, for growth and for ion uptake in roots of Carex diandra and Carex
acutiformis. Physiologia Plantarum, 72: 483–491.
Van Oosten, M.J., A. Sharkhuu, G. Batelli, R. A. Bressan, and A. Maggio, 2013. “The Arabidopsis
thaliana mutant air1 implicates SOS3 in the regulation of anthocyanins under salt stress,” Plant
Molecular Biology, 83:405–415.
Vanlerberghe, G.C., G.D. Martyn, and K. Dahal, 2016. Alternative oxidase: a respiratory electron
transport chain pathway essential for maintaining photosynthetic performance during drought
stress. Physiol Plant., 157:322–337. PMID: 27080742. Doi: 10.1111/ ppl.1245 .
Veeranagamallaiah, G., G. Jyothsnakumari, M. Thippeswamy, P.C.O. Reddy, G.K. Surabhi, G.
Sriranganayakulu, Y. Mahesh, B. Rajasekhar, C. Madhurarekha, and C. Sudhakar, 2008.
Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv) Prasad.
Veiga, T.A.M., S.C. Silva, A.C. Francisco, E.R. Filho, P.C. Vieira, J.B. Fernandes, et al., 2007.
Inhibition of photophosphorylation and electron transport chain in thylakoids by lasiodiplodin,
a natural product from Botryosphaeria rhodina. J. Agricult. Food Chem. 55: 4217–4221. doi:
10.1021/ jf070082b.
Vieira Santos, C.L., A. Campos, H. Azevedo, and G. Caldeira, 2001. In situ and in vitro senescence
induced by KCI. stress: nutritional imbalance, lipid peroxidation and antioxidant metabolism.
J. Exp. Bot. 52, 351–360. doi: 10.1093/jexbot/52.355.351.
Vincent, D., A. Ergül, M.C. Bohlman, E.A. Tattersall, R.L. Tillett, M.D. Wheatley, R. Woolsey, D.R.
Quilici, J. Joets, K. Schlauch, D.A. Schooley, J.C. Cushman, and G.R. Cramer 2007. Proteomic
analysis reveals differences between Vitis. Vinifera L. cv. Chardonnay and cv. Cabernet
Sauvignon and their responses to water deficit and salinity. J. Exp. Bot., 58:1873–1892.
Vorasoot, N., P. Songsri, C. Akkasaeng, S. Jogloy, and A. Patanothai 2003. Effect of water stress on
yield and agronomic characters of peanut. Songklanakarin J. Sci. Technol., 25:283–288.
Wahid, A., R. Rao, and E. Rasul, 1997. Identification of salt tolerance traits in sugarcane lines. Field
Crop Res., 54:9–17.
Walia, A., J.S. Lee, G. Wasteneys, and B. Ellis, 2009. Arabidopsis mitogenactivated protein
kinaseMPK18 mediates cortical microtubule functions in plant cells. Plant J., 59:565–575
Wang, B., U. L¨uttge, and R. Ratajczak, 2001. “Effects of salt treatment and osmotic stress on V-
ATPase and V-PPase in leaves of the halophyte Suaeda salsa,” Journal of Experimental Botany,
52(365):2355–2365.
Wang, M.C., Z.Y. Peng, C.L. Li, F. Li, C. Liu, and G.M. Xia, 2008a. Proteomic analysis on a high salt
tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics,
8:1470–1489.
Wang, S., P. Liu, D. Chen, L. Yin, H. Li, and X. Deng, 2015Silicon enhanced salt tolerance by
improving the root water uptake and decreasing the ion toxicity in cucumber. Front. Plant Sci.,
6, 759. [CrossRef] [PubMed]
Wang, W., B. Vinocur, and A. Altman, 2003. Plant responses to drought, salinity and extreme
temperatures: towards genetic engineering for stress tolerance. Planta, 218:1–14.
Wang, X., P. Fan, H. Song, X. Chen, X. Li, and Y. Li, 2009. Comparative proteomic analysis of
differentially expressed protein in shoots of Salicornia europea, under different salinity. J.
Proteome Res., 8:3331– 3345.
Wang, X., P. Yang, Q. Gao, X. Liu, T. Kuang, S. Shen, and Y. He, 2008b. Proteomic analysis of the
response to high-salinity stress in Physcomitrella patens. Planta, 228:167–177.
Wang, X.S., and J.G. Han, 2007. Effects of NaCl and silicon on ion distribution in the roots, shoots and
leaves of two alfalfa cultivars with different salt tolerance. Soil Sci. Plant Nutr., 53:278–285.
[CrossRef]
Wang, Y. and N. Nii, 2000. “Changes in chlorophyll, ribulose bisphosphate carboxylase-oxygenase,
glycine betaine content, photosynthesis and transpiration in Amaranthus tricolor leaves during
salt stress,” Journal of Horticultural Science and Biotechnology, 75(6):623–627.
Watanabe, M., M. Kusano, A. Oikawa, A. Fukushima, M. Noji, et al., 2008. Physiological roles of the
beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 146: 310-320.

396
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Weisany, W., Y. Sohrabi, G. Heidari, A. Siosemardeh, and K.G. Golezani, 2012. Changes in antioxidant
enzymes activity and plant performance by salinity stress and zinc application in soybean
(Glycine max L). Plant OMICS. 5(2):60–67.
White, P.J., and M.R. Broadley, 2001. Chloride in soils and its uptake and movement within the plant:
a review. Ann. Bot., 88:967–988.
Winicov, I., and J.R. Seemann, 1990. Expression of genes for photosynthesis and the relationship to
salt tolerance of alfalfa (Medicago sativa) cells. Plant Cell Physiol. 31: 1155–1161. doi:
10.1093/oxfordjournals.pcp.a078029.
Wirtz, M., and M. Droux, 2005. Synthesis of the sulfur amino acids: cysteine and methionine.
Photosynth. Res., 86: 345-362.
Witzel, K., A. Weidner, G.K. Surabhi, A. Börner, and H.P. Mock, 2009. Salt stress-induced alterations
in the root proteome of barley genotypes with contrasting response towards salinity. J. Exp.
Bot., 60: 3546–3557.
Wu, D., S. Cai, M. Chen, L. Ye, Z. Chen, H. Zhang, F. Dai, F. Wu, and G. Zhang, 2013. Tissue
metabolic responses to salt stress in wild and cultivated barley. PLoS. One, 8:e55431.
Wu, J., H.-P. Mock, R.F.H. Giehl, B. Pitann, and K.H. Mühling, 2019. Silicon decreases cadmium
concentrations by modulating root endodermal suberin development in wheat plants. J. Hazard.
Mater. 364, 581–590. Doi: 10.1016/j. jhazmat.2018.10.052.
Wu, J., J. Guo, Y. Hu, and H. Gong, 2015. Distinct physiological responses of tomato and cucumber
plants in silicon-mediated alleviation of cadmium stress. Front. Plant Sci., 6, 453. [CrossRef]
Wu, Q.S., and Y.N. Zou, 2009. Adaptive responses of birch-leaved pear (Pyrus betulaefolia. seedlings
to salinity stress. Not. Bot. Horti Agrobot. Cluj Napoca 37: 133–138. doi:
10.15835/nbha3713109.
Wu, X., Z. Zhu, X. Li, and D. Zha, 2012. Effects of cytokinin on photosynthetic gas exchange,
chlorophyll fluorescence parameters and antioxidative system in seedlings of eggplant
(Solanum melongena L). under salinity stress. Acta Physiol. Plant, 34: 2105–2114. [CrossRef]
Wyn, J.R.G., C.J. Brady, and J. Speirs, 1979. Ionic and osmotic relations in plant cells. In: Laidman
DL, W.yn Jones RG. (eds) Recent advances in the biochemistry of cereals. Academic Press,
L.ondon, 63–103.
Xiong, J., G. Fu, L. Tao, and C. Zhu, 2010. “Roles of nitric oxide in alleviating heavy metal toxicity in
plants,” Archives of Biochemistry and Biophysics, 497(1-2):13–20.
Xu, C., T. Sibicky, and B. Huang 2010. Protein profile analysis of salt responsive proteins in leaves and
roots in two cultivars of creeping bent grass differing in salinity tolerance. Plant Cell Rep., 29:
595–615.
Xu, C.X., Y.P. Ma, and Y.L. Liu, 2015. Effects of silicon (Si) on growth, quality and ionic homeostasis
of aloe under salt stress. S. Afr. J. Bot., 98: 26–36. [CrossRef]
Xu, G., H. Magen, J. Tarchitzky, and U. Kafkafi, 2000. Advances in chloride nutrition of plants. Adv
Agron., 68:97–150.
Xu, S., B. Hu, Z. He, F. Ma, J. Feng, W. Shen, and J. Yan, 2011. Enhancement of salinity tolerance
during rice seed germination by presoaking with hemoglobin. Int J. Mol. Sci., 12:2488–2501.
Yadav, S.K., S.L. Singla-Pareek, M. Ray, M.K. Reddy and S.K. Sopory, 2005. Transgenic tobacco
plants overexpressing glyoxalase enzymes resist an increase in methylglyoxal and maintain
higher reduced glutathione levels under salinity stress. FEBS. Letters, 579: 6265-6271.
Yamaguchi, K., Y. Takahashi, T. Berberich et al., 2006. “The polyamine spermine protects against high
salt stress in Arabidopsis thaliana,” FEBS. Letters, 580(30):6783–6788,
Yamaguchi, K., Y. Takahashi, T. Berberich, A. Imai, A. Miyazaki, et al., 2006. The polyamine spermine
protects against high salt stress in Arabidopsis thaliana. FEBS. Lett., 580: 6783-6788.
Yamori, W., 2016. Photosynthetic response to fluctuating environments and photoprotective strategies
under abiotic stress. J. Plant Res. 129: 379–395. [CrossRef]
Yamori, W., 2016. Photosynthetic response to fluctuating environments and photoprotective strategies
under abiotic stress. J. Plant Res., 129: 379–395. [CrossRef]
Yan, A., and Z. Chen, 2019. Impacts of silver nanoparticles on plants: a focus on the phytotoxicity and
underlying mechanism. Int. J. Mol. Sci. 20: 1003.

397
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Yang, Q., Z.Z. Chen, X.F. Zhoua, H.B. Yina, X. Lia, X.F. Xina, X.H. Honga, J.K. Zhu, and Z. Gong,
2009. Over-expression of SOS. (salt overly sensitive. genes increases salt tolerance in
transgenic Arabidopsis. Mol. Plant, 2:22–31.
Yang, Y., and Y. Guo, 2018. Elucidating the molecular mechanisms mediating plant salt-stress
responses. New Phytol., 217: 523–539. [CrossRef]
Yang, Y., and Y. Guo, 2018. Unraveling salt stress signaling in plants. J. Integr. Plant Biol., 60, 796–
804. [CrossRef]
Yano, H., 2014. Ongoing applicative studies of plant thioredoxins. Mol. Plant, 7:4–13. PMID:
23966635. doi:10.1093/mp/sst124.
Yassen, A., E. Abdallah, M. Gaballah, and S. Zaghloul, 2017. Role of silicon dioxide nano fertilizer in
mitigating salt stress on growth, yield and chemical composition of cucumber (Cucumis sativus
L). Int J. Agric Res 12:130–135. https://doi.org/10.3923/ijar.2017.130.135.
Ye, Y., I.A. Medina-Velo, K. Cota-Ruiz, F. Moreno-Olivas, and J.L. Gardea-Torresdey, 2019. Can
abiotic stresses in plants be alleviated by manganese nanoparticles or compounds? Ecotoxicol.
Environ. Saf. 184, 109671. You, J., C.han, Z., 2015. ROS. regulation during abiotic stress
responses in crop plants. Front. Plant Sci. 6, 1092.
Ye, Y., K. Cota-Ruiz, J.A. Hern´andez-Viezcas, C. Vald´es, I.A. Medina-Velo, R.S. Turley, J.R.Peralta-
Videa, and J.L. Gardea-Torresdey, 2020a. Manganese nanoparticles control salinity-modulated
molecular responses in Capsicum annuum L. through priming: a sustainable approach for
agriculture. ACS. Sustain. Chem. Eng. 8: 1427–1436.
Yen, H.E., S.-M. Wu, Y.-H. Hung, and S.-K. Yen, 2000. “Isolation of 3 salt-induced low-abundance
cDNAs from light-grown callus ofMesembryanthemum crystallinum by suppression
subtractive hybridization,” Physiologia Plantarum, 110(3):402– 409.
Yin, J., J. Jia, Z. Lian, Y. Hu, J. Guo, H. Huo, Y. Zhu, and H. Gong, 2019. Silicon enhances the salt
tolerance of cucumber through increasing polyamine accumulation and decreasing oxidative
damage. Ecotoxicol. Environ. Saf., 169: 8–17. [CrossRef]
Yin, L., S. Wang, J. Li, K. Tanaka, and M. Oka, 2013. Application of silicon improves salt tolerance
through ameliorating osmotic and ionic stresses in the seedling of Sorghum bicolor. Acta
Physiol. Plant., 35: 3099–3107. [CrossRef]
Yin, L., S. Wang, K. Tanaka, S. Fujihara, A. Itai, X. Den, and S. Zhang, 2016. Silicon-mediated changes
in polyamines participate in silicon-induced salt tolerance in Sorghum bicolor L. Plant Cell
Environ., 39: 245–258. [CrossRef]
Yiu, J.-C., L.-D. Juang, D. Y.-T. Fang, C.-W. Liu, and S.-J. Wu, 2009. “Exogenous putrescine reduces
flooding-induced oxidative damage by increasing the antioxidant properties of Welsh onion,”
Scientia Horticulturae, 120(3):306–314.
Yokotani, N., T. Ichikawa, Y. Kondou, M.Matsui, H. Hirochika, M. Iwabuchi, and K. Oda, 2009.
Tolerance to various environmental stresses conferred by the salt-responsive rice gene
ONAC063 in transgenic Arabidopsis. Planta, 229:1065–1075.
Yoshida, K., and T. Hisabori, 2014. Mitochondrial isocitrate dehydrogenase is inactivated upon
oxidation and reactivated by thioredoxin-dependent reduction in Arabidopsis. Front. Environ.
Sci., 2:1–7. doi:10.3389/fenvs.2014.00038.
Yoshida, K., K. Noguchi, K. Motohashi, and T. Hisabori, 2013. Systematic exploration of thioredoxin
target proteins in plant mitochondria. Plant Cell Physiol., 54:875–892. PMID: 23444301.
doi:10.1093/pcp/pct037.
Yu, J., S. Chen, Q. Zhao, T. Wang, C. Yang, C. Diaz, G. Sun, and S. Dai, 2011. Physiological and
proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J. Proteome Res 10:3852–
3870.
Zargar, S.M., R. Mahajan, J. A. Bhat, M. Nazir, and R. Deshmukh, 2019. Role of silicon in plant stress
tolerance: opportunities to achieve a sustainable cropping system. 3 Biotech 9:73. Doi:
10.1007/s13205-019-1613-z.
Zargar, S.M., R. Mahajan, J.A. Bhat, M. Nazir, and R. Deshmukh, 2019Role of silicon in plant stress
tolerance: Opportunities to achieve a sustainable cropping system. 3 Biotech., 9, 73. [CrossRef]
Zhang, C.J., B.C. Zhao, W.N. Ge, Y.F. Zhang, Y. Song, et al., 2011. An apoplastic h-type thioredoxin
is involved in the stress response through regulation of the apoplastic reactive oxygen species
in rice. Plant Physiol., 157: 1884-1899.

398
Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Zhang, F., Y. Wang, Y. Yang, H. Wu, D. Wang, and J. Liu, 2007. “Involvement of hydrogen peroxide
and nitric oxide in salt resistance in the calluses from Populus euphratica,” Plant, C.ell and
Environment, 30(7):775–785.
Zhang, J.L. and H. Shi, 2013. “Physiological and molecular mechanisms of plant salt tolerance,”
Photosynthesis Research, 115:1–22.
Zhang, M.H., Z.H. Qin, and X. Liu 2005. Remote sensed spectral imagery to detect late blight in field
tomatoes. Precision Agriculture, 6: 489–508.
Zhang, N.N., H. Zou, X.Y. Lin, Q. Pan, W.Q. Zhang, J.H. Zhang, and J. Chen, 2020. Hydrogen sulfide
and rhizobia synergistically regulate nitrogen N. assimilation and remobilization during N.
deficiency-induced senescence in soybean. Plant Cell Environ. 43: 1130–1147. [CrossRef]
[PubMed]
Zhang, W., W.J. Peumans, A. Barre, C.H. Astoul, P. Rovira, P. Rougé, P. Proost, P. Truffa-Bachi,
A.A.H. Jalali, and E.J.M. van Damme, 2000. Isolation and characterization of a jacalin-related
mannose-binding lectin from salt-stressed rice (Oryza sativa) plants Planta, 210:970–978.
Zhang, W.Q., Y.Z. Huang, and L.J. Zhao, 2009. Effect of silicon on the germination of Si mutant rice
and wild rice seeds under salt stress. Asian J. Ecotoxicol., 4: 867–873.
Zhang, Y., L. Wang, Y. Liu, Q. Zhang, Q. Wei, and W. Zhang, 2006. “Nitric oxide enhances salt
tolerance inmaize seedlings through increasing activities of proton-pump and Na+/H+ antiport
in the tonoplast,” Planta, 224(3):545–555.
Zhao, F., C.P. Song, J. He, and H. Zhu, 2007. Polyamines improve K+/Na+ homeostasis in barley
seedlings by regulating root ion channel activities. Plant physiol., 145: 1061–1072. [CrossRef]
Zhao, G., Y. Zhao, W. Lou, J. Su, S. Wei, X. Yang, R. Wang, R. Guan, H. Pu, and W. Shen, 2019.
Nitrate reductase-dependent nitric oxide is crucial for multi-walled carbon nanotube-induced
plant tolerance against salinity. Nanoscale, 11: 10511–10523.
Zhao, L., B. Peng, J.A. Hernandez-Viezcas, C. Rico, Y. Sun, J.R. Peralta-Videa, X. Tang, G. Niu, L.
Jin, A. Varela-Ramirez, J.Y. Zhang, and J.L. Gardea-Torresdey, 2012. Stress response and
tolerance of Zea mays to CeO2 nanoparticles: cross talk among H2O2, heat shock protein and
lipid peroxidation. ACS. Nano 6:9615–9622. https://doi.org/10.1021/nn302975.
Zhao, L., F. Zhang, J. Guo, Y. Yang, B. Li, and L. Zhang, 2004. “Nitric oxide functions as a signal in
salt resistance in the calluses from two ecotypes of reed,” Plant Physiology, 134(2):849– 857.
Zhao, X., P. Wei, Z. Liu, B. Yu, and H. Shi, 2017. Soybean Na+/H+ antiporter GmsSOS1 enhances
antioxidant enzyme activity and reduces Na+ accumulation in Arabidopsis and yeast cells under
salt stress. Acta Physiol. Plant., 39, 19. [CrossRef]
Zhou, J., F. Li, J. Wang, Y. Ma, K. Chong, and Y. Xu, 2009. Basic helix-loophelix transcription factor
from wild rice (OrbHLH2) improves tolerance to salt and osmotic stress in Arabidopsis. J. Plant
Physiol., 166: 1296–1306.
Zhu Z., G. Wei, J. Li, Q. Qian, and J. Yu, 2004. “Silicon alleviates salt stress and increases antioxidant
enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L)” Plant Science,
167(3):527–533.
Zhu, J.K. 2004. Plant salt tolerance and the SOS. pathway. In: Proceedings of the XLVIII. Italian
Society of Agricultural Genetics: SIFV-SIGA. Joint Meeting, L.ecce, I.taly (15–18 September,
2004) I.SBN. 88- 900622-5-8.
Zhu, J.K., 2001. Plant salt tolerance. Trends Plant Sci., 6:66–71.
Zhu, J.-K., 2003. “Regulation of ion homeostasis under salt stress,” CurrentOpinioninPlant Biology,
6(5): 441–445.
Zhu, J.K., 2016. Abiotic stress signaling and responses in plants. Cell, 167: 313–324. [CrossRef]
Zhu, J.K., J. Liu, and L. Xiong, 1998. Genetic analysis of salt tolerance in Arabidopsis. Evidence for a
critical role of potassium nutrition. Plant Cell, 10:1181–1191.
Zhu, Y.X., and H.J. Gong, 2014. Beneficial effects of silicon on salt and drought tolerance in plants.
Agron. Sustain. Dev., 34: 455–472. [CrossRef]
Zhu, Y.-X., G. Hai-Jun and Y. Jun-Liang, 2019. Role of Silicon in Mediating Salt Tolerance in Plants:
A Review, Plant s, 8, 147; doi: 10.3390/plants8060147 www.mdpi.com/journal/plants
Zhu, Y.X., H.J. Gong, and J.L. Yin, 2019a. Role of silicon in mediating salt tolerance in plants: a review.
Plants 8:147. Doi: 10.3390/plants8060147.

299
 Middle East J. Appl. Sci., 12(3): 282-400, 2022
EISSN: 2706 -7947 ISSN: 2077- 4613 DOI: 10.36632/mejas/2022.12.3.27

Zhu, Y.X., J. Guo, R. Feng, J.H. Jia, W.H. Han, and H.J. Gong, 2016. The regulatory role of silicon on
carbohydrate metabolism in Cucumis sativus L. under salt stress. Plant Soil, 406: 231–249.
[CrossRef]
Zhu, Y.X., X.B. Xu, Y.H. Hu, W.H. Han, J.L. Yin, H.L. Li, and H.J. Gong, 2015. Silicon improves salt
tolerance by increasing root water uptake in Cucumis sativus L. Plant Cell Rep., 34: 1629–
1646. [CrossRef]
Zhu, Z., G. Wei, J. Li, Q. Qian, and J. Yu, 2004. Silicon alleviates salt stress and increases antioxidant
enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L). Plant Sci., 167: 527–
533. [CrossRef]
Zhu, Z.J., G.Q. Wei, J. Li, Q.Q. Qian, and J.Q. Yu, 2004. Silicon alleviates salt stress and increases
antioxidant enzymes activity in leaves of saltstressed cucumber (Cucumis sativus L). Plant Sci.,
167:527–533.
Zi, Z., W. Liebermeister, and E. Klipp, 2010. A quantitative study of the Hog1 MAPK. Response to
fluctuating osmotic stress in Saccharomyces cerevisiae. PLoS. One 5:e9522.
Ziaf, K., M. Amjad, M.A. Pervez, Q. Iqbal, I.A. Rajwana, and M. Ayyub, 2009. Evaluation of different
growth and physiological traits as indices of salt tolerance in hot pepper (Capsicum annuum L).
Pakistan J. Bot. 41: 1797–1809.
Zorb, C., C.-M. Geilfus and K.-J. Dietz, 2019. Salinity and crop yield, Plant Biology 21 (Suppl. 1. 31–
38) 2018 German Society for Plant Sciences and The Royal Botanical Society of the
Netherlands.
Zörb, C., R. Herbst, C. Forreite, and S. Schubert, 2009. Short-term effects of salt exposure on the maize
chloroplast protein pattern. Proteomics, 9: 4209–4220.
Zörb, C., S. Schmitt, and K.H. Mühling, 2010. Proteomic changes inmaize roots after short-term
adjustment to saline growth conditions. Proteomics, 10:4444–4449.
Zulfiqar, F., and M. Ashraf, 2021. Nanoparticles potentially mediate salt stress tolerance in plants.
Plant Physiol. Biochem. 160: 257–268.

400

View publication stats