1405

Salt stress changes biochemical, physiological and photosynthetic attributes of

Satureja spicigera

Hoshang Rahmati*1 and Borzou Yousefi2

1.Department of Agriculture, Technical and Engineering Faculty, Payam Noor University, Tehran, Iran,
2.Kermanshah Agricultural and Natural Resources Research and Education Center, Kermanshah, Iran
________________________________________________________________________________

Abstract

We investigated the effect of salt stress on photosynthetic, physiological, and biochemical traits of Satureja
spicigera (C. Koch) Boiss., a medicinal plant used in edible products and healthcare industries. The experiment
was designed in a randomized complete block design (RCB) with three replications in a greenhouse. The salt
treatments included four levels of NaCl (0, 50, 100, and 150 mM). Results showed that salinity levels caused
a significant reduction in some photosynthetic, morpho-physiological, physiological, and biochemical
characteristics; however, it boosted antioxidant activity. Salinity levels significantly reduced leaf fresh weight
(12.56%), leaf dry weight (18.53%), relative water content (11.94%), chlorophyll a (33.33%), chlorophyll b
(15.62%), chlorophyll a+b (29.24%), and carotenoid content (42.46%). However, salinity significantly boosted
the antioxidant activity of superoxide dismutase (236.50%), peroxidase (85.67%), and catalase (82.78%) on
average. Salt stress also significantly increased proline content (373.33%), protein content (84.49%), and leaf
electrical conductivity (333.26%) on average. Results confirm that S. spicigera tolerates NaCl concentrations
below 100 mM; however, it is highly sensitive to NaCl concentrations above 100 mM, so that a salinity of 150
mM causes a dramatic decrease in photosynthesis and growth. Therefore, we do not recommend the
cultivation of this plant in highly saline and semi-saline soils.

Keywords: Antioxidant activity, Medicinal plants, Photosynthesis, Salt stress.

Abbreviation: C: control; Car: carotenoid; CAT: catalase; Chl: chlorophyll; LFW: leaf fresh weight; LDW: leaf
dry weight; LTW: Leaf turgor weight; OD: optical density; POD: peroxidase; Pro: proline; ROS: reactive oxygen
species; RWC: relative water content; SOD: superoxide dismutase.

Rahmati, H. and B. Yousefi, 2024. Salt stress changes biochemical, physiological and photosynthetic
attributes of Satureja spicigera. Iranian Journal of Plant Physiology 14 (4), 5257- 5264.
_____________________________________________________________________________

Introduction
Abiotic stresses affect the biosynthesis of primary absorption, causing ionic imbalance, and leading
and secondary metabolites in plants (Jan et al., to membrane and photosynthetic damage
2021). Salinity stress interrupts the growth and through excessive ROS production
development of crops by reducing water (Balasubramaniam et al., 2023), which negatively
impacts food security. Under salinity stress, the
____________________________________
* Corresponding Author
production of large amounts of ROS causes
E-mail Address hoshang.rahmatipnu@pnu.ac.ir oxidative stress, which harms cell membranes and
Received: May, 2024 cellular function. The enzymatic antioxidant
Accepted: August, 2024
5258 Iranian Journal of Plant Physiology, Vol (14), No (4)

defense scavenges ROS by converting superoxide intensity), followed by 7 hours of darkness

into H2O, which helps plants tolerate oxidative (Hernández-Adasme et al., 2023), with a relative
stress (Afridi et al., 2019). Salt stress also adversely humidity of 50-60%. Each pot was irrigated twice
affects photosynthetic pigments (Mohammadi et a week with 2500 ml of well water. Four
al., 2019; Zarei et al., 2019) and osmotic treatments were implemented, involving
adjustment (Zhang et al., 2013). Proline, as a ROS irrigation (250 ml per pot, twice a week) with 0, 50,
scavenger (Kumar et al., 2017), and salt stress 100, and 150 mM NaCl (Kumar et al., 2022). We
proteins (Athar et al., 2022) have a prominent removed the accumulated salts from the pots with
effect on cell osmotic adjustment in response to distilled water after every four irrigations with the
salinity stress. Plant growth and development NaCl treatments.
usually decrease due to the adverse effects of
salinity on photosynthesis and related processes Morpho-physiological Measurements
(Saadatfar and Jafari, 2024; Zarei et al., 2019).
Throughout history, humankind has used aromatic We measured leaf fresh weight (LFW), leaf turgor
plants in medicine and cooking. Recently, weight (LTW), and leaf dry weight (LDW) using 30
medicinal plants have attracted the attention of young leaves from each plant. These young leaves
chemists, pharmacists, and botanists for their were immediately weighed with precision (0.0001
potential roles as alternatives to synthetic g) (LFW). The leaves were immersed in double-
pharmaceuticals(Ahad et al., 2021; Kulak, 2020). distilled water for 18 hours to reach full hydration
The Lamiaceae family is one of the most important (22 °C). After drying the leaf surfaces, they were
families of medicinal plants (Kulak, 2020), weighed again (LTW). The leaves were then placed
containing more than 6000 species with a global in an oven (70 °C, 48 h), and the leaf dry weight
distribution. Satureja spicigera is a perennial (LDW) was measured. The means of LFW and LDW
medicinal plant belonging to the Lamiaceae family were calculated in grams (g). RWC was calculated
that grows in rocky places in northern and north- using the following formula (Bian and Jiang, 2009):
western Iran. Native people use this plant as a
food additive and vegetable. This plant is also used RWC (%) = (LFW–LDW)/(LTW–LDW)100
in food, pharmaceutical, and health industries.
There is limited data on the effect of salinity stress Photosynthetic Assays
on this plant. This experiment was carried out to
explore the possibility of growing this plant in low Chlorophyll a, b, and carotenoid content were
and semi-saline soils. measured. The samples were centrifuged for 10
minutes (10000 rpm, 4 °C), and the supernatant
Materials and Methods was measured at 663, 646, and 470 nm using a
microplate reader. The content of photosynthetic
Experimental Design and Treatments pigments (mg g⁻¹ FW) was calculated using the
following formulas (Lichtenthaler and Wellburn,
A greenhouse experiment with three replications, 1983):
based on a randomized complete block design
(RCB), was carried out at the Research Center for Chl a = 12.21 (A663) – 2.81 (A646)
Agricultural and Natural Resources in
Kermanshah, Iran. Seeds were disinfected with Chl b = 20.13 (A646)– 5.1 (A663)
0.5% sodium hypochlorite, washed, and dried.
They were planted in a peat moss bed and Chl T = Chl a + Chl b
watered by sprinkling. The seedlings were
Carotenoid = (1000 A470 – 3.27 [Chl a] – 104 [Chl b]/227)
transferred to plastic pots (one seedling per pot),
filled with a mixture of farm soil, sand, and
Biochemical Assays
composted cow manure. The plants were
maintained under a 17-hour light photoperiod
The extraction buffer and crude leaf extract were
with 300 μmol/m²s (equivalent to 110 lux of light
prepared (Reddy et al., 2004). The enzymatic
 Physiological and Biochemical Alterations in Satureja spicigera under Salt Stress 5259

Table 1

Analysis of variance of photosynthetic pigments, proline content, protein content, RWC, LFW, LDW, and SOD, POD, and
CAT activities in S. spicigera under different NaCl or, and NSe treatment.

S.O.V. df Chl a Chl b Carotenoid Chl a+b Proline

Salt 3 34.99** 1.70 ** 2.82 ** 51.50 ** 0.07**
Error 6 0.28 0.08 0.05 0.58 0.02
CV (%) 6.07 8.52 8.78 5.68 17.74

S.O.V. df Soluble protein Relative water content SOD POD CAT

Salt 3 2384.00** 114.3 ** 5.79 ** 16.94** 7.39**
Error 6 1.22 16.5 0.02 0.1 0.013
CV (%) 0.17 4.79 7.38 12.54 2.95
* and **= significant differences at the level of 0.05 and 0.01, respectively and Ns = no significant difference

activity rate of superoxide dismutase (SOD, EC Statistical Analysis

1.15.1.1) was measured based on the ability of
SOD to stop the photochemical reduction of Analysis of variance and Duncan's Test (p < 0.05)
nitroblue tetrazolium (NBT) by superoxide radicals were performed using IBM SPSS Statistics 26
in the presence of riboflavin under light conditions software. The charts were created using Excel
(Beauchamp and Fridovich, 1971). The optical software.
absorbance was read at 560 nm (one enzymatic
unit equals 50% inhibition) using a microplate Results
reader. The activity of SOD was calculated using
the following formula: The results of ANOVA revealed significant
differences (p < 0.01) for chlorophyll a, b,
(OD control−OD sample)
−1
100 − [
OD control
] × 100 carotenoid, chlorophyll a + b, proline, soluble
SOD(µmol g FW) =
50 protein, relative water content, and SOD, POD,
and CAT activities (Table 1).
where:
 OD control: absorbance of control at 560 Photosynthetic Pigments
nm
 OD sample: absorbance of samples at 560 The highest chlorophyll a (12.90 mg g⁻¹ FW), b
nm (3.67 mg g⁻¹ FW), a + b (15.86 mg g⁻¹ FW), and
carotenoid (3.87 mg g⁻¹ FW) were observed in the
The peroxidase (POD; E.C. 1.11.1.7) activity was non-NaCl-treated plants. Salinity treatments
measured using a microplate reader and significantly decreased, on average, the amounts
expressed in terms of H₂O₂ consumption (μmol of chlorophyll a, b, carotenoid, and chlorophyll a +
min⁻¹ mg⁻¹ of soluble protein) (Chance and b by 33.33%, 15.62%, 42.46%, and 29.24%,
Maehly, 1955). The optical absorbance was respectively (Fig. I). The highest photosynthetic
recorded for 15 minutes at 30-second intervals at performance index (2.86) was observed in the
a wavelength of 470 nm, and calculated using the control plants. Salt treatments significantly
Beer-Lambert law (0.0266 M⁻¹cm⁻¹). The activity of reduced this trait by an average of 35.31% (Fig. II).
catalase (CAT; E.C. 1.11.1.6) was measured (Sinha,
1972) with some modifications, using the Beer- Antioxidant Activity
Lambert law (extinction coefficient of 0.0394
M⁻¹cm⁻¹). Proline content was measured (Bates et The highest SOD (3.64 µmol min⁻¹ mg⁻¹ protein),
al., 1973) as well as soluble protein concentration POD (3.05 µmol min⁻¹ mg⁻¹ protein), and catalase
(mg g⁻¹ FW) (Bradford, 1976).
5260 Iranian Journal of Plant Physiology, Vol (14), No (4)

Fig I. Means comparison of chlorophyll a, chlorophyll b, carotenoid, and total chlorophyll (a + b) content
in Satureja spicigera plants in response to different NaCl treatments. Columns with the same letters are
not significantly different based on LSD test (Mean ± SD, p = 0.05).

Fig.II. Means comparison (LSD Means ±SD) for photosynthetic performance index, superoxide
dismutase, peroxidase, and catalase activity of Satureja spicigera plants in response to different NaCl
treatments. The same letters are not show significant difference (P= 0.05).
activity (4.69 µmol min⁻¹ mg⁻¹ protein) were µS cm⁻¹) was observed in the plants treated with
observed in plants treated with 150 mM NaCl (Fig. 150 mM NaCl (Fig. III b). Salinity significantly
II). Salinity levels significantly increased SOD, POD, decreased the leaf fresh weight by 12.56%, leaf
and catalase activity, on average, by 236.50%, dry weight by 18.53%, and leaf relative water
85.67%, and 82.78%, respectively, compared to content by 11.94% in the salt-treated plants
the control plants (Fig. II). compared to the control (Fig. III a, b). Salinity
significantly increased LEC by 333.26% in the salt-
The highest leaf fresh weight (12.31 mg) and leaf treated plants compared to the control (Fig. III b).
dry weight (2.45 mg) were observed in the plants
treated with 50 mM NaCl (Fig. III a). The highest Morpho-Physiological and Physiological
RWC (89.13%) was observed in the non-NaCl- Attributes
treated plants; however, the highest LEC (378.23
 Physiological and Biochemical Alterations in Satureja spicigera under Salt Stress 5261

NaCl 0 mM NaCl 50 mM
a RWC (%) LEC (μs/cm)
NaCl 100 mM NaCl 150 mM
400
14.00 ab a 300
12.00 bc 200
10.00 c
8.00 100
6.00 0
4.00 NaCl 0 NaCl 50 NaCl 100 NaCl 150
a a ab
b mM mM mM mM
2.00
0.00 Fig IV. Relationship between relative water content
Leaf fresh weight Leaf dry weight (RWC) and leaf electrical conductivity (LEC) of
Satureja spicigera plants during enhancement NaCl
(mg) (mg)
concentration.

b NaCl 0 mM NaCl 50 mM
NaCl 100 mM NaCl 150 mM
NaCl 0 mM NaCl 50 mM
500
NaCl 100 mM NaCl 150 mM
a
400 1.5
a a a
300 1 b b
d c
b c
0.5
200
a b c c 0
100 c c Proline (µg g-1 Protein (mg g-1
FW) FW)
0
RWC (%) LEC (μs/cm) Fig. V. Means comparison (LSD Mean’s ± SD) leaf
proline content and leaf protein content of Satureja
Fig III. Means comparison (LSD Mean’s ± SD): (a) leaf spicigera plants in response to different NaCl
fresh weight and leaf dry weight, (b) relative water treatments. The same letters are not show significant
content (RWC) and leaf electrical conductivity (LEC) of difference (P= 0.05).
Satureja spicigera plants in response to different NaCl
treatments. The same letters are not show significant
difference (P= 0.05).

Biochemical Traits
The relationship between the leaf relative water
content and the electrical conductivity is inverse. Salt levels severely increased proline content. The
Its trend can be seen in Fig. IV. This relationship highest proline (1.08 µg g⁻¹ FW) was observed in
shows that under salinity stress greater than 50 150 mM NaCl (Fig. V). Salt levels significantly
mM, the relative water content decreases with a increased proline content by 373.33% on average.
gentle and uniform slope, but the electrical The 50 and 100 mM NaCl treatments caused a
conductivity increases with a very steep slope. severe rise in protein content (112% on average)
compared to the control; however, 150 mM NaCl
5262 Iranian Journal of Plant Physiology, Vol (14), No (4)

improved the protein content by 30.23% the other NaCl treatments. Similar to these
compared to the control (Fig. V). results, low salinity treatments increased soluble
protein, while high levels of NaCl significantly
Discussion declined it in Thymus vulgaris (Harati et al., 2015).

In salt-sensitive plants, chlorophyll concentration Salinity reduces turgor pressure and interrupts the
decreases significantly at high levels of NaCl; ionic balance between the plant and soil (Wang et
however, in salt-resistant plants, the al., 2023). Therefore, salinity strongly affects the
concentration of chlorophyll is less affected by salt plant's water status. The relative water content
stress(Srivastava and Sharma, 2021). In the significantly decreased in response to different
present study, different NaCl levels caused a levels of NaCl; however, leaf electrical
significant decrease in Chl a, Chl b, total Chl, conductivity significantly increased. Similar to
carotenoid content, and the performance index of these findings, RWC significantly decreased in
photosynthesis. Similar to our findings, salinity response to different salt concentrations in Lemon
significantly decreased chlorophyll a and b in verbena (Ghanbari et al., 2023)and Oryza sativa
Satureja hortensis (Mohammadi et al., 2019)and (Jini and Joseph, 2017).
Satureja khuzestanica (Saadatfar and Jafari, 2024),
as well as carotenoid content in Satureja hortensis In the present study, NaCl caused a significant
(FABRIKI and MEHRABAD, 2016). decrease in leaf fresh weight and leaf dry weight.
A high salt concentration in the root zone reduces
Under oxidative stress, enzymatic antioxidant the osmotic potential of water in the surrounding
activity increases and scavenges excessive ROS. roots. Therefore, the plant's access to water is
These enhanced enzymatic activities ameliorate reduced. A lack of water in the plant causes partial
oxidative damage caused by stressful agents closure of the stomata, thus reducing the entry of
(Garcia-Caparros et al., 2021). In the present CO₂ into the plant (Shanker et al., 2022). Reducing
research, the antioxidant activity of SOD, POD, and the absorption of CO₂ in plants diminishes
CAT significantly increased in response to NaCl photosynthesis and growth. Salinity causes ion
concentrations. In S. khuzestanica, different NaCl toxicity (in the form of Na⁺ and Cl⁻). A high
levels significantly increased the activity of SOD, concentration of Na⁺ decreases nitrate reductase
POD, and CAT (Saadatfar and Jafari, 2024). These activity and inhibits the functioning of
results confirm our findings. photosystem II ((Sheldon et al., 2017), which leads
to a decrease in plant growth. Additionally, salinity
In plants under osmotic stress, the accumulation causes nutrient deficiency (N, P, K, Zn, and Fe),
of proline and other osmoprotectants increases. In which decreases plant growth and development
the present research, the proline content (Sheldon et al., 2017).
significantly augmented in response to salt levels.
Similar to our findings, salinity levels significantly The destruction of cell membranes due to salt is
increased the proline content in Satureja hortensis associated with a diminution in the absorption and
(Mohammadi et al., 2019), Satureja khuzestanica transfer of nutrients through the roots, a decrease
(Saadatfar and Jafari, 2024), and Thymus danensis in the biosynthesis of chlorophyll, and an increase
(Harati et al., 2015). in the destruction of chlorophyllase due to salinity,
which causes a decrease in plant growth and
Low salt levels stimulate plant growth and cause development.
the synthesis of de novo proteins; however, high
salinity levels reduce the synthesis of proteins Conclusion
(Zhang et al., 2013). Also, a part of the proteins is
decomposed in response to high salt (Hao et al., The present study confirms that S. spicigera, to
2021). Different salt levels caused a significant some extent, tolerates concentrations of less than
increase in the protein content; however, this 100 mM NaCl, but it is highly sensitive to
increase was limited at 150 mM NaCl compared to concentrations greater than 100 mM NaCl, such
 Physiological and Biochemical Alterations in Satureja spicigera under Salt Stress 5263

that a salinity of 150 mM causes a significant Therefore, we do not recommend the cultivation
decrease in photosynthesis and growth. of this plant in saline or semi-saline soil.

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