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Plant-Derived Smoke Solution: A Stress Alleviator in Crop

Article in Journal of Plant Growth Regulation · January 2024

DOI: 10.1007/s00344-023-11221-7

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Journal of Plant Growth Regulation
https://doi.org/10.1007/s00344-023-11221-7

Plant‑Derived Smoke Solution: A Stress Alleviator in Crop

Muhammad Mudasar Aslam1 · Amana Khatoon2 · Muhammad Jamil3 · Shafiq Ur Rehman4 · Setsuko Komatsu5

Received: 20 June 2023 / Accepted: 7 December 2023

© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2024

Abstract
Plant-derived smoke is known as a potent agent to promote plant growth at different developmental stages. The application of
plant-derived smoke elicits germination and post-germination stages of plant species. On the other hand, abiotic stresses, such
as salinity, heavy metals, and flooding, are known to weaken plant growth and development. Abiotic stresses have negative
effects on growth attributes of crops, such as maize, rice, wheat, and soybean. The positive/alleviating effect of plant-derived
smoke solution was observed at morphological, physiological, and molecular levels of plant under abiotic stresses. Presently,
the role of plant-derived smoke in alleviation of various stresses including salt, heavy metal, temperature, and flooding stress
has been comprehended and the mechanism of alleviation via regulation of cellular activities at molecular level has been
discussed. The amelioration of negative effects of abiotic stresses by plant-derived smoke involves the regulation of stress-
related genes that provokes the antioxidant system of plants, activating cell wall proteins and metabolic pathways that might
block the uptake of salt/heavy metal ions through plant roots. This review might provide an in-depth role of plant-derived
smoke to exploit new avenues enabling plants to cope with abiotic stresses.

Keywords Plant-derived smoke solution · Stress alleviator · Crop

Abbreviations
PDS Plant-derived smoke
APX Ascorbate peroxidase
POD Peroxidase
Handling Editor: Václav Motyka. CAT​ Catalase
SOD Superoxide dismutase
* Setsuko Komatsu MDA Malondialdehyde
skomatsu@fukui-ut.ac.jp
ABA Abscisic Acid
Muhammad Mudasar Aslam KAR Karrikin
mudasar_kust@yahoo.com
ROS Reactive oxygen species
Amana Khatoon TSS Total soluble sugar
amanakhatoon@kust.edu.pk
TSP Total soluble proteins
Muhammad Jamil GR Glutathione reductase
jamilkhattak@yahoo.com
GABA Gamma amino butyric acid
Shafiq Ur Rehman H2O2 Hydrogen peroxide
drshafiq@yahoo.com
Pb Lead
1
Department of Botany, University of Science Hg Mercury
and Technology, Bannu 28100, Pakistan As Arsenic
2
Department of Botany, Kohat University of Science &
Technology, Kohat 26000, Pakistan
3
Department of Biotechnology & Genetic Engineering, Kohat Introduction
University of Science & Technology, Kohat 26000, Pakistan
4
Department of Biology, University of Haripur, Plant-derived smoke generated during fire is a well-known
Haripur 22620, Pakistan agent for promoting plant growth and development (Kamran
5
Faculty of Environment and Information Sciences, Fukui et al. 2017), and positively affects plant species of different
University of Technology, Fukui 910‑8505, Japan

Vol.:(0123456789)
 Journal of Plant Growth Regulation

habitats (van Staden et al. 2006). Seed germination cues (Chumpookam et al. 2012). These results suggest that plant-
associated with fire or post-fire environments were identified derived smoke solution improved physiological attributes
as heat, temperature, chemicals, and smoke (Baxter et al. in plants.
1994; Paul et al. 2007). Smoke produced during fire was Abiotic stress is an environmental factor, which can limit
recognized as a major germination cue in post-fire environ- plant growth and productivity (Nabi et al. 2019). Due to the
ments (Brown 1993). Species related to a fire-prone environ- continuous climate change and environmental deterioration
ment positively respond to smoke produced during forest fire induced by human activity and physical surroundings, stress
(Brown 1993; Todorovic et al. 2005). Plant-derived smoke has become a key threat to plant life (Tandzi et al. 2019). The
enhanced the germination process in plant communities impact of abiotic stresses on plants has been observed from
such as the South African Mediterranean (Light et al. 2002; morphological to molecular levels and is visible in all phases
Brown et al. 2003) and Californian chaparral (Keely and of plant development (Fahad et al. 2017). Different abiotic
Fotheringham 1998). It can re-establish plant communities stresses affect the plants due to global warming and fluctua-
in semi-arid regions, such as chaparral in southern Califor- tions in the environmental conditions. Abiotic stresses, like
nia (Todorovic et al. 2005), fynbos in South Africa (Light salinity, extreme temperatures, and heavy metal toxicities,
et al. 2002), and Kwongan in Australia (Brown et al. 2003). significantly reduce the productivity of crop (Yadav et al.
It is clear that plant-derived smoke affects seed germination 2020). Abiotic stresses are interrelated and influence cer-
and establishes different plant communities. tain reactions in plant resulting in a series of changes that
Plant-derived smoke is a promising factor for several affect growth and diversity (Krasensky and Jonak 2012).
growth-related phenomena of plants including breaking Plant morphological responses to abiotic stresses include
seed dormancy, accelerating seed germination, and increas- decreased seed germination, reduced seedling growth, wilt-
ing seedling growth (Aslam et al. 2017, 2019; Rehman et al. ing/abscission of the leaves, and lower plant yield (Fghire
2018). Plant-derived smoke solution showed maximum et al. 2015). Abiotic stress delays metabolism, dissipates
enhancement of seed germination in plant species (Schwilk energy, and causes free radicals to form as a result of oxida-
and Zavala 2012). Plant-derived smoke solution significantly tive stress (Farooq et al. 2009). These findings demonstrated
promoted seed germination in Arabidopsis and lettuce by the dynamic negative effects of abiotic stresses on morpho-
increasing the activity of hydrolytic enzymes, which sup- logical and physiological attributes of plants.
ports the mobilization of stored food reserves (Nelson et al. The promising question or idea has been now developed
2011; Kamran et al. 2013; Khatoon et al. 2020). Positive from the above-mentioned investigations that whether plant-
effects of plant-derived smoke solution at post-germination derived smoke solution can improve plant growth under dif-
level were observed in crops, such as rice (Jamil et al. 2014; ferent stress conditions? In this context, several studies have
Malook et al. 2017), wheat (Aslam et al. 2015), and maize been carried out to evaluate the role of plant-derived smoke
(van Staden et al. 2006; Aslam et al. 2017). Plant-derived in amelioration of detrimental effects of salinity, heavy met-
smoke solution treatments improved seedling development, als toxicity, and flooding stress in crops such as rice (Akhtar
seedling length/mass, root cuttings, pollen germination, et al. 2017), sorghum (Khan et al. 2014), soybean (Li et al.
pollen tube growth, and crop yield in okra (Kulkarni et al. 2018; Zhong et al. 2020), and wheat (Aslam et al. 2015;
2007a), acacia (Kulkarni et al. 2007b), maize (Aslam et al. Catav et al. 2021; Hayat et al. 2021; Ibrahim et al. 2022).
2019), ipomoea cuttings (Aslam et al. 2014), and mem- This review highlights the role of plant-derived smoke solu-
bers of Amaryllidaceae family (Kumari et al. 2015). These tion in the presence of abiotic stresses and focusses the pos-
findings suggest that plant-derived smoke enhanced plant sible mechanism of crop growth in response to plant-derived
growth and development. smoke solution under abiotic stresses.
Plant-derived smoke solution enhanced biochemical
growth attributes in different plant species. Photosynthetic
pigments, like chlorophyll contents, total nitrogen, total Composition of Plant‑Derived Smoke
soluble proteins, and photosynthetic rates, increased under Solution
plant-derived smoke treatments (Jamil et al. 2014). Total
soluble sugar, α-amylase activity, starch, protein contents, The positive effects of plant-derived smoke are mainly due to
lipase activity, and lipid contents increased in lettuce plant the presence of compounds obtained during burning of plant
treated with plant-derived smoke solution (Gupta et al. species. Till date, compounds isolated from plant-derived
2019). Photosynthetic pigments, total phenolics, total fla- smoke are butenolide (Flematti et al. 2004), 3, 4, 5-trimeth-
vonoids, and proanthocyanidins increased in Tulbaghia spe- ylfuran-2(5H)-one (Light et al. 2010), glyceronitrile or
cies treated with plant-derived smoke solution (Aremu et al. cyanohydrin (Flematti et al. 2011), Catechol (Wang et al.
2012). Plant-derived smoke has positive effects on nutri- 2017a, b), Hydroquinone (Kamran et al. 2017), 5,5-dimeth-
ents, like nitrogen and Fe/Zn/Cu ions in papaya seedlings ylfuran-2(5H)-one, and (5RS)-5-ethylfuran-2(5H)-one
Journal of Plant Growth Regulation

(Burger et al. 2018). There are six analogues of butenolides 2009). A second phase takes place over days or even weeks
different with respect to methyl substitutions (Flematti et al. and pertains to the build-up of cytotoxic ion levels, which
2007). Butenolide or karrikin derived from plant-derived slows down metabolic processes, causes premature senes-
smoke is a well-known seed germination agent (van Staden cence, and ultimately cell death (Roy et al. 2014). Tolerance
et al. 2004). Besides having promoting effects on seed ger- to both phases is governed by a multitude of physiological
mination, karrikins are phytoreactive compounds with appli- and molecular mechanisms: osmotic tolerance, ionic toler-
cations in horticulture, ecological restoration, and agricul- ance, and tissue tolerance (Roy et al. 2014). Osmotic toler-
ture (Dixon et al. 2009). ance initiates relatively quickly and includes a rapid decrease
Cyanohydrin is another compound isolated from plant- in stomatal conductance to preserve water (Maathuis et al.
derived smoke solution. The positive activities of cyanohy- 2014). These results suggest that salt stress altered morpho-
drin compound are dependent on the spontaneous release of logical as well as physiological aspects of plants.
cyanide (Flematti et al. 2011). Cyanide-stimulated germina-
tion is common in a wide variety of plant species (Flematti
et al. 2011). Besides these, some of the compounds present Effect of Plant‑Derived Smoke on Seed Germination,
in plant-derived smoke solution have negative effects on Seedling Length, and Fresh Weight Under Salt Stress
plant growth (van Staden et al. 2004). Trimethyl butenolides
or 3,4,5-trimethyl-2(5H)-furanone isolated from smoke solu- Rice-seed germination decreased with the increase in salt
tion have inhibitory effects on seed germination (Light et al. concentrations; however, priming with plant-derived smoke
2010). The inhibitory effects of 3, 4, 5-trimethyl-2(5H)-fura- solution showed better seed germination than the salt-treated
none are only reported in lettuce seeds (Light et al. 2010). ones (Jamil et al. 2014; Malook et al. 2014). Plant-derived
Furthermore, inhibitory compounds, 5, 5-dimethylfuran- smoke solution treatments enhanced rice-seed germina-
2(5H)-one and (5RS)-5-ethylfuran-2(5H)-one, are isolated tion in the presence of salt stress. Maize seeds primed with
from red oat grass and skilpadbessie-derived smoke solu- Cymbopogon-derived smoke solution significantly enhanced
tion, respectively (Burger et al. 2018). The presence of this seed germination (Waheed et al. 2016). Seed germination
diverse nature compounds in plant-derived smoke might be percentage in wheat seeds treated with 150 and 200 mM
the reason behind the variable growth responses of plants to NaCl was restored to quite big extent in the presence of
smoke solution. 2000 ppm smoke solution (Hayat et al. 2022). Results sug-
gest that application of plant-derived smoke solution can
potentially alleviate the salt stress in wheat at germination
Salinity Stress level even at higher salt concentrations i.e. 150 and 200 mM
(Fig. 1; Table 1).
Effects of Salt Stress on Plant Morphological Positive effects of plant-derived smoke solution have been
and Biochemical Attributes observed at the seedling stage under salt stress conditions.
Salt stress gradually reduced shoot and root length of maize
Salinity is a major threat to agriculture causing inhibition (Waheed et al. 2016); and plant-derived smoke solution
and impairment of crop growth and development. Salinity alleviated these negative effects of 50, 100, 150 mM salt
is one of severe problems, which negatively affects crop concentrations on rice shoot/root lengths (Jamil et al. 2014).
productivity (Taffouo et al. 2009). Salinity stress weakens Malook et al. (2014) reported better shoot and root lengths in
plant growth and development via water stress, cytotoxic- Basmati-385 when treated with 200 and 1000 ppm bauhinia-
ity due to excessive uptake of ions such as sodium (­ Na+), derived smoke dilution under different concentrations of salt
chloride ­(Cl−), and nutritional imbalance. Salinity stress has stress. Waheed et al. (2016) documented that plant-derived
negative effects on plant morphological growth characters smoke solution significantly reduced the drastic effects of
including seed germination, seedling length/biomass, leaves different salt concentrations on the lengths of maize seed-
water potential, and turgor pressure (Arif et al. 2020). It has lings. Catav et al. (2021) reported that seedling length of
negative effects on physiochemical parameters including wheat decreased by 150 mM salt stress was recovered when
photosynthetic contents andprotein/sugar contents in black 1000 ppm plant-derived smoke solution was applied along
gram and maize (Kapoor and Srivastava 2010; Waheed et al. with salt stress. Seedling length in wheat was reduced by
2016). Salinity is typically accompanied by oxidative stress 150 and 200 mM NaCl but application of 2000 ppm plant-
due to the generation of reactive-oxygen species (ROS) derived smoke solution significantly improved wheat shoot/
(Isayenkov 2012). Plant responses to salinity are divided root length in the presence of salt stress (Hayat et al. 2022).
into two main phases. An ion-independent growth reduction, It is concluded from the mentioned literature that plant-
which takes place within minutes to days, causes stomatal derived smoke significantly reduced the effects of salt stress
closure and inhibition of cell expansion (Rajendran et al. in numerous plant species.
 Journal of Plant Growth Regulation

Fig. 1  A schematic diagram

showing responses of plant to Leaf area/biomass/ diameter
plant-derived smoke solution Chlorophyll a/b, carotenoids
in the presence of salinity, CAT, APX, POD,SOD Shoot length/ biomass,
heavy metals, flooding, and
temperature stress. Left) Effects
relative water contents
of plant-derived smoke solution Total nitrogen, protein Na+
on seed germination in the pres- and phenolics K+, Ca+2
ence of salinity, heavy metals, Seed amylase
flooding, and temperature stress.
contents
Right) Effects of plant-derived Root hair
smoke solution on morphologi-
cal and physiological param-
eters in the presence of salinity,
heavy metals, and flooding
stress Total nitrogen, Root length/biomass,
protein and phenolics secondary roots
contents
Na+
CAT, APX, POD, SOD
K+, Ca+2

Seed germination

Similar to seed germination and seedling length, plant- salt concentrations. Decrease in K ­ + and C
­ a2+ ions while
derived smoke solution increased seedling fresh biomass increase in ­Na+ ions were recorded with increasing salt con-
of rice (Jamil et al. 2014; Malook et al. 2014) and maize centrations from 50 to 150 mM. However, rice seeds primed
(Waheed et al. 2016). Results indicated that 50, 100, and with different plant-derived smoke solutions significantly
150 mM NaCl significantly reduced fresh weight of rice increased ­K+ and C­ a2+ ions while decreased N ­ a+ ions com-
seedling (Jamil et al. 2014; Malook et al. 2014). Plant- pared to rice seeds primed with salt concentrations (Malook
derived smoke solution treatments restored rice and maize et al. 2017). Higher K­ +, ­Ca2+ ions and lower N
­ a+ ions were
growth in the presence of salt stress (Jamil et al. 2014; found in plants grown from seeds primed with 2000 ppm
Malook et al. 2014; Waheed et al. 2016). Better fresh weight bauhinia-derived smoke solution under salt concentra-
of rice seedling was obtained when 2000 ppm plant-derived tions (Waheed et al. 2016). Plant-derived smoke extracts
smoke was used combined with 50, 100, and 150 mM NaCl alleviated significantly the adverse effects of 100, 150, and
(Jamil et al. 2014). Wheat seedling fresh and dry mass were 200 mM NaCl at ionic level (Table 2).
also recovered by 1000 ppm plant-derived smoke solution
under 150 mM NaCl treatment (Catav et al. 2021). Results Effect of Plant‑Derived Smoke Solution
showed that plant-derived smoke improved seedling biomass on Photosynthesis, Total Nitrogen, and Protein
in NaCl-treated plants (Fig. 2). Contents Under Salt Stress

Effect of Plant‑Derived Smoke on Physiochemical Photosynthetic pigments play a key role in the process of
Parameters Under Salt Stress food synthesis in plant leaves. Salt stress is observed as an
agent having negative effects on different photosynthetic pig-
Significant changes were observed in ­Na+, ­K+, and ­Ca2+ ments in plant leaves. It was found that 100, 150, 200, and
ionic contents in rice treated with plant-derived smoke and 250 mM NaCl significantly reduced chlorophyll a, b and
Journal of Plant Growth Regulation

Table 1  Effects of plant-derived smoke solution on morphological growth parameters of different plants
Alleviation solution concentrations Morphological parameters Results References
studied

Rice
2000 ppm PDS + 50 Seed germination, seedling Increased Jamil et al. (2014)
mM NaCl length, root fresh/dry
weights
1000 ppm PDS + 50 mM NaCl shoot fresh weight, shoot Increased Jamil et al. (2014)
dry weight
2000 ppm Cymbopogan-derived smoke solution Seed germination, seedling Increased Malook et al. (2014)
+ 100 mM NaCl length, seedling fresh
1000 ppm Buhania-derived smoke solution + 50 mM NaCl weight
200 ppm PDS + 50 mM NaCl Shoot fresh/dry weight Increased Malook et al. (2017)
200 ppm PDS + 150 mM NaCl Root fresh/dry weight Increased Malook et al. (2017)
1000 ppm PDS + 500 ppm Pb Root length/fresh Increased Akhtar et al. (2017)
weight
2000 ppm PDS + 1500 ppm Pb Root dry weight Increased Akhtar et al. (2017)
Maize
2500 ppm PDS + 100 Seed germination, seedling Increased Waheed et al. (2016)
mM NaCl length
2500 ppm PDS + 150 Mm NaCl Root/shoot fresh and dry Increased Waheed et al. (2016)
weight
Soybean
2000 ppm + flooding stress Root length, root fresh Increased Otori et al. (2020)
weight
2000 ppm PDS + flooding stress Root length, hypocotyl Increased Li et al. (2018)
length
2000 ppm PDS + flooding stress Number of lateral roots, Increased Zhong et al. (2020)
root length
2000 ppm Euclaptus-derived smoke + 10 ppm Boron Seed germination, shoot/ Increased Khan et al. (2014)
stress root length, shoot fresh
weight root fresh/dry
weight
Sweet potato cuttings
2000 ppm PDS + 10 ppm Cobalt stress Number of adventitious Increased Aslam et al. (2014)
roots, numbers of lateral
roots, adventitious root
length
Blue lupin line/cultivar
PDS + 7 °C Seed germination vigour Increased Płazek et al. (2018)
PDS + 13 oC
Wheat
1000 ppm PDS + 150 mM Seedling length, root/shoot ratio (length), seedling dry Increase Catav et al. (2021)
NaCl weight, root/shoot ratio (dry weight)
2000 ppm PDS + 2 mM As Seed germination, shoot length, root length, root fresh Increase Ibrahim et al. (2022)
weight, shoot fresh weight
2000 ppm PDS + 2 mM Hg Seed germination, shoot length, root length, root fresh Increase Ibrahim et al. (2022)
weight, shoot fresh weight
10,000 ppm PDS + 12 mM Root length, total seedling length, root dry weight, total Increased Küçükakyüz and Çatav
Boron seedling dry weight (2021)

carotenoid contents in maize leaves (Waheed et al. 2016). increased chlorophyll “a” and “b” contents than 50, 100,
Alleviation solution of plant-derived smoke and salt con- and 150 ppm NaCl primed seedlings (Jamil et al. 2014).
centrations restored chlorophyll a/b and carotenoid contents Chlorophyll a/b and carotenoid were reduced by 150 mM
in maize leaves affected by NaCl concentrations (Waheed salt stress but 1000 ppm plant-derived smoke treatment
et al. 2016). Plant-derived smoke-primed plants seedlings recovered photosynthetic pigments in wheat leaves (Catav
 Journal of Plant Growth Regulation

Fig. 2  Effects of plant-derived

smoke solution on plant cellular
activities in the presence of
salinity, heavy metals, flooding,
and temperature stress. Upward Cell wall proteins
and downward arrows indicate ATPs contents/ abundance
increased and decreased differ-
ent growth processes, respec-
Cell membrane stability
tively
Glutathione
reductase
Zn,
Proline
H2O2,
MDA,
TBARS
Glycince
betaine
Free amino acids
Lipid peroxidation Chlorophyll a/b
Boron and Lead Carotenoids
Contents RuBisCO activase
Cellular injury RuBisCO large subunit
Water potential RuBisCO small subunit
Osmotic potential
Dehydrogenase, amylase,
Ferritin Bowman-Birk
proteinase isoinhibitor
D-II, Fructokinase enzymes

et al. 2021). These findings suggest that application of plant- causes cellular oxidative stress and damage plants cells
derived smoke solution increased photosynthetic contents in (Ayala et al. 2014). Accumulating evidences have increas-
the presence of NaCl stress (Table 3). ingly shown that stress-tolerant plants produce high amounts
Protein is the main component of many structural units of antioxidant enzymes such as APX, POD, and SOD to
and function of plant body, while nitrogen is the main part eliminate excess amount of ROS in plant cell. SOD detoxi-
of amino acid. Protein and nitrogen contents were decreased fies ­H2O2 by enhancing the levels of APX, POD, and CAT
in rice seedlings in the presence of increasing NaCl con- (Mullineaux et al. 2010; Chen et al. 2013). The contents of
centrations from 50 to 150 mM (Malook et al. 2014; Jamil free radical were reported to be increased in maize seedlings
et al. 2014). Maize seedling treated with NaCl concentra- under salt stress conditions as compared to normal condi-
tions has lower quantity of nitrogen and protein contents tions (Waheed et al. 2016). In short, it is proved that plant-
(Waheed et al. 2016). Plant-derived smoke-treated rice and derived smoke solution ameliorates abiotic stress conditions
maize seedling have better nitrogen and protein contents in by activating ROS-scavenging enzymes.
the presence of NaCl stress (Jamil et al. 2014; Waheed et al. Plant-derived smoke solution reduces ­H2O2 contents in
2016). Among smoke dilutions, 2000 and 2500 ppm signifi- maize seedlings under stress via increasing the activities of
cantly increased nitrogen and protein contents in rice and APX and POD enzymes (Waheed et al. 2016). ­H2O2 and
maize seedlings (Malook et al. 2014; Waheed et al. 2016). lipid peroxidase contents were significantly lowered in wheat
These findings suggest that salt stress-induced changes were seedlings treated with plant-derived smoke under salt stress
alleviated by treatment with plant-derived smoke solution. suggesting that plant-derived smoke plays a significant role
in ROS scavenging (Hayat et al. 2021). Plant-derived smoke
Effect of Plant‑Derived Smoke, Salt Stress, increased the levels of antioxidant enzymes under salt stress,
and Alleviation Solution on Antioxidant Enzymes which may partly explain why plant-derived smoke-treated
wheat plantlets were more resistant to salt stress (Hayat
ROS and lipid peroxidation along with H
­ 2O2 are considered et al. 2021). Plant-derived smoke restored cellular activities
as an important marker of cell damage in plants (Nita et al. by increasing antioxidants enzymes and decreasing H ­ 2O 2
2016). Abiotic stresses accumulate ROS in the cell, which and lipid peroxidation during salt stress. Salinity promoted
Journal of Plant Growth Regulation

Table 2  Effects of plant-derived smoke solution on physiological parameters of different plants

Alleviation solution concentrations Biochemical parameters studied Results References

Rice
2000 ppm PDS + 100 mM NaCl K+, ­Ca++, chlorophyll a, b, carotenoid contents Increased Jamil et al. (2014)
200 ppm PDS + 150 mM NaCl Nitrogen and protein contents Increased Jamil et al. (2014)
2000 ppm PDS + 100 mM NaCl Na+ Decreased Jamil et al. (2014)
2000 ppm Cymbopogan- derived smoke solu- Proline content Decreased Jamil et al. (2013)
tion + 100 mM
NaCl
2000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
1000 ppm Cymbopogan- derived smoke solu- Zn Decreased Jamil et al. (2013)
tion + 50 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
1000 ppm Cymbopogan- derived smoke solu- Cd Decreased Jamil et al. (2013)
tion + 150 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 150 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Pb Decreased Jamil et al. (2013)
tion + 100 mM NaCl
2000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
1000 ppm Cymbopogan- derived smoke solu- Chlorophyll a, b, carotenoids Increased Jamil et al. (2013)
tion + 50 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Chl b Increased Jamil et al. (2013)
tion + 100 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 100 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Carotenoids Increased Jamil et al. (2013)
tion + 50 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Cellular injury Decreased Malook et al. (2014)
tion + 50 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Na+ Decreased Malook et al. (2014)
tion + 100 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 100 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- K+ Increased Malook et al. (2014)
tion + 100 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 50 mM NaCl
2000 ppm Cymbopogan- derived smoke solu- Ca++ Increased Malook et al. (2014)
tion + 50 mM NaCl
1000 ppm Buhania-derived smoke solu-
tion + 100 mM NaCl
200 ppm PDS + 100 Na+ (root/shoot) Decreased Malook et al. (2017)
mM NaCl
200 ppm PDS + 150 K+ (root/shoot) Increased Malook et al. (2017)
mM NaCl
2000 ppm PDS + 500 ppm Pb Total nitrogen content Increased Akhtar et al. (2017)
1000 ppm PDS + 1000 ppm Pb ­ a+, ­Ca++, ­K+
Total protein content, N Increased Akhtar et al. (2017)
+
2000 ppm PDS + 1500 ppm Pb Na Decreased Akhtar et al. (2017)
1000 ppm PDS + 500 ppm Pb Pb content Decreased Akhtar et al. (2017)
 Journal of Plant Growth Regulation

Table 2  (continued)
Alleviation solution concentrations Biochemical parameters studied Results References

1000 ppm PDS + 1000 ppm Pb Proline, glycine betaine Decreased Akhtar et al. (2017)
Maize
2500 ppm PDS + 150 mM NaCl Chlorophyll a, b Increased Waheed et al. (2016)
2500 ppm PDS + 250 mM NaCl Carotenoid content Increased Waheed et al. (2016)
2500 ppm PDS + 200 mM NaCl K+, ­Ca+ Increased Waheed et al. (2016)
10,000 ppm PDS + 100 mM NaCl Total protein content Increased Waheed et al. (2016)
2500 ppm PDS + 100 mM NaCl Total nitrogen content Increased Waheed et al. (2016)
10,000 ppm PDS + 150 mM NaCl Na+ Decreased Waheed et al. (2016)
Soybean
2000 ppm PDS + flooding stress ATP abundance, ATP contents, ascorbate peroxi- Increased Otori et al. (2020)
dase
Sorghum
2000 ppm PDS + 10 ppm Boron Total Boron content (shoot) Decreased Khan et al. (2014)
2000 ppm PDS + 5 ppm Boron stress Total Boron content (roots) Decreased Khan et al. (2014)
Blue lupin line/cultivar
PDS + 7 °C PDS + 13 °C Dehydrogenase activity, amylase activity Increased Płazek et al. (2018)
Wheat
1000 ppm PDS + 150 mM NaCl Proline contents, ­H2O2 contents, MDA contents Decreased Catav et al. (2021)
1000 ppm PDS + 150 mM NaCl Total protein content, total flavonoid content, Increased Catav et al. (2021)
total phenolic content
2000 ppm PDS + 2 mM As Chlorophyll a, b, carotenoids Increased Ibrahim et al. (2022)
2000 ppm PDS + 2 mM Hg Chlorophyll a, b, carotenoids Increased Ibrahim et al. (2022)
2000 ppm PDS + 2 mM As H2O2, lipid peroxidation, TBARS Decreased Ibrahim et al. (2022)
2000 ppm PDS + 2 Mm Hg H2O2, lipid peroxidation, TBARS Decreased Ibrahim et al. (2022)
2000 ppm PDS + flooding stress Chlorophyll contents Increased Komatsu et al. (2022)
4000 ppm PDS + 12 mM Boron Glutathione reductase Decreased Küçükakyüz and Çatav (2021)
10,000 ppm PDS + 12 mM Boron H2O2, MDA, boron content Decreased Küçükakyüz and Çatav (2021)

Table 3  Effects of plant-derived smoke solution on molecular parameters of different plants

Alleviation solution concentrations Molecular parameters studied Results References

Maize
10,000 ppm PDS + 150 mM NaCl POD Decreased Waheed et al. (2016)
2500 ppm PDS + 150 mM NaCl APX Decreased Waheed et al. (2016)
2500 ppm PDS + 200 mM NaCl CAT​ Decreased Waheed et al. (2016)
Soybean
2000 ppm PDS + flooding stress Ferritin, Bowman–Birk proteinase isoin- Increased Li et al. (2018)
hibitor D-II, Fructokinase enzymes
Wheat
2000 ppm PDS + 2 mM As SOD, POD, APX, CAT​ Decreased Ibrahim et al. (2022)
2000 ppm PDS + 2 mM Hg SOD, POD, APX, CAT​ Decreased Ibrahim et al. (2022)
4000 ppm PDS + 12 mM Boron POD, SOD, APX, CAT​ Decreased Küçükakyüz and Çatav (2021)
2000 ppm + PDS flooding stress RuBisCO activate, RuBisCO large subu- Increased Komatsu et al. (2022)
nit, RuBisCO small subunit

ROS production through the over-reduction of the electron different parts of seedlings during growth (Sunmonu et al.
transport chain in chloroplasts and induced lipid peroxida- 2016) and that ­H2O2 and MDA contents can decrease or
tion (Cheng et al. 2020). The available studies suggest that remain unchanged in response to low concentrations of the
plant-derived smoke has mixed effects on MDA content in smoke solution under a stress condition (Akhtar et al. 2017).
Journal of Plant Growth Regulation

Catav et al. (2021) proved that 1000 ppm plant-derived (Shah et al. 2020). Karrikins receptor gene KAI2 could up-
smoke solution was not enough to alter the levels of ­H2O2 regulate the expression of DERB2A, EFR5, and WRKY33
and MDA in wheat seedlings in the absence or presence under abiotic stress and thus regulate plant growth (Wang
of salt stress. Studies have revealed that plants synthesize et al. 2018). These findings suggest that karrikin compound
a high quantity of CAT, APX, POD, and SOD in order to which is derived from smoke solution regulates stress-
eliminate ROS by converting them to less toxic form. PDS- related proteins to reduced salt stress.
treated seedlings have an increased level of antioxidants as Another school of thought believed that smoke solution-
compared to control and stressed plants (Shah et al. 2020). derived compound karrikins enhanced seed germination in
These results suggests that plant-derived smoke solution Eragrostis tef (zucc.) under osmotic stress by modulating
activated plant immune system to cope with abiotic stresses. GA biosynthesis-related genes, boosting ROS-scavenging
antioxidant enzymes and sugar mobilization in seeds (Sun-
Mechanism of Alleviation of Salt Stress Through monu et al. 2016; Shabir et al. 2021). KAR1 was used to
Plant‑Derived Smoke Solution at Morphological promote seed germination and seedling vigour in tomato
Level under salt stress (Jain and van Staden 2007). It is suggested
that plant-derived smoke and karrikins could regulate
Plant-derived smoke solution is a powerful growth restor- some physiological processes and control ion homeostasis
ing agent against different abiotic stresses. The exit mecha- in maize seeds and thus alleviate salt stress and improved
nism of restoring morphological growth of different crops seed germination (Iqbal et al. 2013). KAR1-treated plants
by plant-derived smoke under salt stress is not clear. There have lowered MDA and ­H2O2 contents under osmotic or
are different theories related to the alleviation of different salt stresses (Shah et al. 2020). Karrikinolide derived from
stresses through plant-derived smoke. According to one plant-derived smoke has shown stimulatory effects on seed
school of thought, plant-derived smoke solution reduced germination as KAR1-treated seeds were found to have max-
the expression of stress-related genes and activated phenolic imum carbohydrate content. According to Sunmonu et al.
pathways which play key role in the increasing of resistance (2016), seedling growth was improved due to the break-
in plant against stresses (Rehman et al. 2018). Plant-derived down of starch found in seed as well as increased activity
smoke compounds also significantly induced the accumula- of amylase enzyme in roots and above ground parts. KAR1
tion of stress-related secondary metabolites and the expres- is involved in seedling growth as it up-regulates the auxins
sion of stress-responsive genes and ABA signalling genes, biosynthetic pathways. Therefore, the variability in growth
which contributed to improved stress tolerance in Sapium is probably due to the crosstalk between KAR1-regulated
sebiferum seedlings (Shah et al. 2020). Stress-resistant auxin production which ultimately affects growth (Nelson
plants have developed a specific molecular mechanism to et al. 2010; Banerjee et al. 2019). These findings confirm
cope with undesirable conditions (Bandurska 2022). There that plant-derived smoke and karikins activated the meta-
are specific genes such as SOS1 (Salt Overly Sensitive 1), bolic pathways and reduced the expression of stress-related
SOS4, HKT2, P3CS, and BADH, DREB2A (Dehydration- genes to overcome salt-induced stress in plants.
Responsive Element-Binding Protein 2A), ERF6 (Ethylene Plant-derived smoke solution also restored physiological
Reception Factor 6), and WRKY33, which are reported as growth parameters including photosynthetic pigments, nitro-
osmotic and salt stress regulatory genes (Yinglu et al. 2019). gen, and protein contents of crops deteriorated by salt stress.
Overexpression of BADH and HKT2 have secured plants Besides these, plant-derived smoke also increases activities
from salt stress (Ni et al. 2018). Plant-derived smoke sig- of antioxidants enzymes to cope with different stresses. It is
nificantly enhanced the expression levels of SOS4, HKT2, believed that plant-derived smoke causes structural proteins
P3CS, and BADH under salt stress (Hayat et al. 2021). These cleavage in order to accumulate secondary metabolite accu-
findings suggest that plant-derived smoke solution protects mulation in plant species to combat stress condition (Iqbal
plant from the toxic effects of stresses by regulating differ- et al. 2018). Plant-derived smoke solutions possess essential
ent mechanisms. nutrient elements like Ca, Mg, K, N, Fe, Mn, and Cu neces-
Arabidopsis DREB2 genes were found to be involved in sary for the syntheses of photosynthetic pigments, enzymes,
osmotic and salt stress resistance and regulate the expres- proteins, and other biochemical growth compounds (Irfan
sion of stress-responsive genes (Nakashima et al. 2000). The 2011). It is also thought that plant-derived smoke may be
SOS1 family proteins were reported as salt stress regula- involved in the synthesis of protein by increasing the absorp-
tory proteins in the Arabidopsis (Shi et al. 2000). Ethylene tion of growth nutrients (Aslam et al. 2017). Malook et al.
response factor-6 was found to be involved in abiotic stress (2014) reported that priming seeds with smoke solution
resistance via the regulation of ROS signalling in Arabidop- enhanced synthesis of chlorophyll and carotenoid contents
sis (Sewelam et al. 2013). KAR1 significantly up-regulated by decreasing the accumulation of N ­ a+ ion. Smoke priming
these stress-related genes under osmotic and NaCl stresses decreased the accumulation of toxic ions like ­Na+ and C­ l− by
 Journal of Plant Growth Regulation

increasing the absorption and accumulation of useful ions Zn, Hg, and As are for long being accumulated in soils
including ­K+ and ­Ca+2 in rice (Jamil et al. 2014). It is also through anthropogenic activities such as industrial waste,
possible that plant-derived smoke may activate the enzymes fertilizer applications, smelting, and sewage disposal (Aydi-
which are responsible for changes in the membrane perme- nalp and Marinova 2009). These activities cause leaching of
ability, due to which the transport of N ­ a+ may be reduced metals into groundwater or accumulate them on soil surface
+
in plant, which ultimately enhances ­K content (Jamil et al. (Ozturk et al. 2017; Basheer 2018). All heavy metals are
2013). Thus, it is believed that plant-derived smoke solution non-biodegradable that is why they cannot be removed natu-
uses different ways to reduce salt stress in plants. rally from the environment via any possible natural means.
The application of KAR1 improved chlorophyll synthesis Although some of them are reported to be immobile, so they
in carrot and incited photosynthetic activity with the increase cannot be moved from the place where they are accumu-
in stomatal conductance and ­CO2 concentration (Akeel et al. lated, while there are others that are termed as mobile that
(2019). Plant-derived smoke-primed seeds had a higher can be taken up by plant root system via diffusion, endo-
number of nuclei than hydro-primed seeds in tomato, which cytosis, or through metal transporters (Alharbi et al. 2018;
helped in higher growth values under stress conditions such Burakova et al. 2018). Nevertheless, some of these metals
as salinity (Jain and van Staden 2007). KAR1-treated seed- such as zinc, copper, and nickel are essential micronutrients
lings have increased levels of enzymatic antioxidants under and are required in trace amounts because they act as cofac-
osmotic and drought stresses, which may partly explain why tors for enzymes. While other metals such as cadmium and
KAR1-treated plants were more tolerant to abiotic stresses lead present in pesticides do not have any beneficial role
(Shah et al. 2020). Overall, the predominant increase of the and become toxic if their concentration exceeds a certain
antioxidants and the reduction of H ­ 2O2, MDA, and electro- limit (Ali et al. 2016, 2017). Thus, it is proven that heavy
lyte leakage emphasized the role of karrikins in maintaining metals are added to nature through many ways and pollute
the redox homeostasis and in the prevention of oxidative the natural environment.
damage during abiotic stress acclimation (Shah et al. 2020). Heavy metal stress has severe effects on plant morpho-
ABA is an essential phytohormone in the regulation of abi- logical, physiological, and biochemical growth attributes. It
otic stress adaptation (Lee and Luan 2012). KAR1 signifi- inactivates or denatures important enzymes and other pro-
cantly reduced the ABA level, under osmotic or salt stress, teins and interferes with substitution reactions of essential
and several ABA signalling genes, such as ABI3 and ABI5, metal ions from biomolecules (Hossain et al. 2012). This
were differentially regulated by KAR1 treatment (Shah et al. reaction disturbs the integrity of membranes, resulting in
2020). ABA stimulates several changes in plant physiologi- alteration of basic plant metabolic reactions such as photo-
cal, molecular, and developmental progressions, resulting in synthesis, respiration, and homeostasis (Hossain et al. 2012).
plant adaptation to the stress environment (Ton et al. 2009). Moreover, it stimulates the production of ROS such as super-
Antioxidant enzymes such as ascorbate peroxidase, catalase, oxide radical (­ O−2), hydroxyl radical (OH), and hydrogen
peroxidase, and superoxide dismutase activated by KAR1 peroxide ­(H2O2) (Barconi et al. 2011). Another cytotoxic
protect cell apoptosis by scavenging the ROS and mitigating compound called methylglyoxal has also been reported to
biotic and abiotic stresses (Sunmonu et al. 2016). Smoke increase during heavy metal stress. These highly reactive
solution and karrikinolide have shown stimulatory activity species lead to lipid peroxidation, especially of the cellu-
on hydrolytic enzymes such as lipases and α-amylase under lar membranes causing them to leak, damaging of biomol-
all conditions such as in the presence of red light, far-red ecules and cleavage of DNA strands (Ahmad et al. 2012).
light, and dark (Gupta et al. 2019). It is confirmed that plant- The mentioned literature reveals that heavy metals stress
derived smoke solution treatment reduced the drastic effects disturbs plant growth by activating ROS and other cytotoxic
of salt stress at physiological level by activating metabolic compounds.
enzymes and synthesis of essential organic and inorganic
compounds. Effect of Plant‑Derived Smoke on Plant Growth
Under Heavy Metal Stress

Heavy Metals Plant-derived smoke is not commonly studied along with

heavy metals. A study revealed that 10, 20, and 30 ppm
Effects of Heavy Metals on Morphological ­CoCl2 concentrations significantly inhibited the number
and Physiological Activities in Plants of adventitious roots, number of lateral roots, and length
of adventitious roots (Aslam et al. 2014). It was observed
Plants in nature constantly encounter with abiotic stresses that higher concentrations of C
­ oCl2 induced more inhibi-
including temperature, water, drought and specifically heavy tory effects on the number of adventitious roots, lateral
metal stress. Heavy metals such as Fe, Mn, Cu, Ni, Co, Cd, roots, and adventitious roots length of ipomoea cutting
Journal of Plant Growth Regulation

compared to lower concentration (Aslam et al. 2014). On As stress (Akhtar et al. 2017; Ibrahim et al. 2022). SOD
the other hand, 2000 ppm plant-derived smoke increased and POD contents increased in rice and wheat seedlings
the number of adventitious roots, lateral roots, and adventi- with increasing Pb, Hg, and As concentrations while smoke
tious roots length of Ipomoea cutting (Aslam et al. 2014). treatment reduced the level of SOD and POD. Catalase and
Boron stress inhibited morphological growth characteris- ascorbate peroxidase contents were significantly affected
tics including seed germination, seedling length/weight, and by Pb, Hg, and As concentrations in rice and wheat seed-
number of secondary roots in sorghum (Khan et al. 2014). ling (Akhtar et al. 2017; Ibrahim et al. 2022). Plant-derived
Smoke solution prepared from five different plants has sig- smoke treatments recovered rice and wheat seedlings from
nificantly improved growth in sorghum plant (Khan et al. the drastic effects of Pb, Hg, and As stress and maintained
2014). Plant-derived smoke application recovered ipomoea balance level of CAT and APX (Akhtar et al. 2017; Ibrahim
and sorghum growth in the presence of ­CoCl2 and boron et al. 2022). Malondialdehyde (MDA) and Hydrogen perox-
stress. Plant-derived smoke application increased morpho- ide ­(H2O2) contents increased with increasing Pb concentra-
logical growth parameters in ipomoea and sorghum plants tion in the roots of rice while smoke priming reduced the
in the heavy metals stress (Aslam et al. 2014; Khan et al. level of MDA and ­H2O2 in the roots of rice cultivars (Akhtar
2014). It is possible that plant-derived smoke solution might et al. 2017). These results confirm that plant-derived smoke
reduce the uptake of heavy metals through roots and thus solution restored rice from the negative effects of Pb stress
decrease the drastic effects on ipomoea and sorghum plants by stimulating physiological growth attributes.
(Aslam et al. 2014; Khan et al. 2014). These results suggest
that plant-derived smoke mitigates heavy metals stress and Mechanism of Alleviation of Heavy Metal Through
restores plant growth. Plant‑Derived Smoke Solution at Morphological
Level
Effect of Plant‑Derived Smoke on Physiochemical
Parameters Under Heavy Metal Stress Land degradation and soil contamination are a persistent
threat to humans’ and the environment’s wellbeing (Azam
Plant-derived smoke were applied on rice roots in the pres- 2016). Heavy metals in soil have increased rapidly in.
ence of Lead (Pb) stress to determine Pb contents, electro- terms of natural phenomena and anthropogenic activi-
lytes contents, total soluble sugar, total soluble protein, and ties, including mining, agricultural activities, and indus-
antioxidant enzymes (Akhtar et al. 2017). Pb contents in trial and municipal discharge, which all pose severe threats
rice roots were significantly increased with increasing Pb to environmental protection (Sharma et al. 2021). Heavy
stress. Pb contents in rice roots were significantly reduced metals such as Cd, Cu, Pb, and Zn often coexist in con-
by the application of plant-derived smoke solution-primed taminated soils and their mobility and bioavailability are
treatments (Akhtar et al. 2017). Electrolyte (­ Na+2, ­Ca+2, ­K+) of global concern due to uptake in plants and increasing
contents were significantly reduced by increasing Pb stress human exposure through food (Tchounwou et al. 2012).
(Akhtar et al. 2017). Plant-derived smoke solution-primed Plant roots are the first organ which comes in direct contact
treatment 1000 ppm increased values of N ­ a+, ­Ca+2, ­K+ elec- with different heavy metal pollutants (Jahangir et al. 2008).
trolytes in rice roots. Pb stress has significantly deteriorated Akhtar et al. (2017) reported that Pb stress induced negative
total soluble sugar (TSS) and total soluble proteins (TSP) changes in root length, root fresh/dry weight of rice varieties
in root rice (Akhtar et al. 2017). Plant-derived smoke treat- (Akhtar et al. 2017). However, application of plant-derived
ments decreased proline content while enhanced total solu- smoke solution alleviated these changes in roots under Pb
ble sugar at 1000 ppm in rice under Pb stress. Photosynthetic stress. Rice root growth inhibition under Pb toxicity is due
pigments are the most fundamental and basic ingredients in to inhibition of nitrate reductase activity and cell division
the photosynthesis process, and hence, play a crucial part in (Eun et al. 2000). Plant-derived smoke enhanced growth by
the creation of plant food (Farooq et al. 2020). Mercury (Hg) boosting nutrient reserves through improved physiological
and Arsenic (As) stress significantly reduced photosynthetic performance and root proliferation under heavy metal stress
pigments in wheat (Ibrahim et al. 2022). Chlorophyll a, b conditions (Khan et al. 2014). These results confirm that
and carotenoids contents were significantly decreased by plant-derived smoke solution significantly reduced the nega-
Hg and As treatments (Ibrahim et al. 2022). Plant-derived tive effects of heavy metal stress in plants.
smoke treatments ameliorated the drastic effects of Hg and Plant-derived smoke containing butenolides acts as a
As on photosynthetic pigments in wheat leaves. stimulant for root growth under stress condition (Sparg
Similarly, different antioxidant enzymes including super- et al. 2005; Jamil et al. 2014). Pb stress strongly influ-
oxide dismutase (SOD), peroxidase (POD), catalase (CAT), ences mineral nutrition, ionic assimilation, and acquisi-
and ascorbate peroxidase (APX) were studied in rice and tion in plants (Kosobrukhov et al. 2004). Seregin et al.
wheat treated with plant-derived smoke under Pb, Hg, and (2004) reported that Pb stress induced electro leakage
 Journal of Plant Growth Regulation

in maize roots which has damaging effects on cell mem- Effect of Plant‑Derived Smoke on Seedling Length
brane. Plant-derived smoke application reduced the and Biomass of Soybean Under Flooding Stress
activity of protein degradation process in rice roots
(Akhtar et al. 2017). It was observed that smoke prim- The growth of soybean seedlings was suppressed by flood-
ing decreased ­H2O2 content and reduced Pb stress. Khan ing but recovered when exposed to plant-derived smoke.
et al. (2014) observed that boron stress significantly The length of the soybean root and hypocotyl was signifi-
reduced morphological growth of sorghum but combined cantly reduced by flooding treatment (Li et al. 2018). When
the solution of plant-derived smoke and boron solution exposed to plant-derived smoke during flooding, though,
recovered sorghum growth. It was suggested that plant- the length of the root and hypocotyl was recovered, and
derived smoke is involved in physiological and metabolic was longer (Li et al. 2018). Main root length decreased
activities that improves plant growth under boron stress by flooding stress; however, significantly increased by the
condition (Khan et al. 2014). Similarly, alleviating effects addition of plant-derived smoke under flooding stress (Otori
of plant-derived smoke solution against boron stress is et al. 2020). Furthermore, root growth of soybean was sig-
just because smoke has the potential to reduce the uptake nificantly reduced during flooding stress but plant-derived
of boron which ultimately leads to tolerance in sorghum smoke treatment recovered the lateral roots growth of soy-
against boron stress (Khan et al. 2014). These results sug- bean. Weight of the root and hypocotyl of flooded soybean
gest that plant-derived smoke solution mitigated heavy was 76 and 46% lower, respectively, than normally growing
metals stress in rice and sorghum. soybean (Li et al. 2018). The weight of root and hypocotyl
treated with plant-derived smoke was 30 and 22% higher,
respectively, than the flooded soybeans. Although growth
of soybean without smoke treatment was inhibited under
Flooding Stress flooding stress, however, this reduction was minimized
in smoke-treated seedlings under flooding stress (Li et al.
Effects of Flooding Stress on Plant Growth 2018). Root fresh weight was decreased by flooding stress;
however, plant-derived smoke significantly increased root
Global climate change and variations in the pattern of fresh weight under flooding stress (Otori et al. 2020). The
precipitation are linked events, which offer necessary length of root including hypocotyl from smoke-treated soy-
ground for flooding to occur worldwide (Zhou et al. beans increased compared to that from untreated plants.
2020). Flooding, as a natural uproar, has detrimental However, the weight of root including hypocotyl did not
impact on terrestrial flora and badly hit crop and forage change (Zhong et al. 2020). In this study, the length and
output globally (Zhou et al. 2020). Water is the essen- weight of wheat leaves were increased by the application of
tial need of all plants, but flooding or excessive water- plant-derived smoke under flooding stress. Morphological
ing causes stress and halts the flow of gases between parameters including leaf length, leaf-fresh weight, main-
the soil and the atmosphere causing anoxia and hypoxia root length, and total-root fresh weight were decreased under
(Zhang et al. 2016). Prolonged flooding events have an flooding stress; however, the application of plant-derived
exceedingly harmful impact on nearly all growth phases smoke solution restored leaf length and leaf-fresh weight
of plant, which ultimately leads to yield loss (Herzog even under flooding (Komatsu et al. 2022). It is concluded
et al. 2016; Striker and Colmer 2017). Flooding typically from the mentioned literature that growth reduction due to
causes plants to experience submergence or partial sub- flooding stress was minimized by PDS.
mergence stress, which has a substantial impact on agri-
cultural production, upsetting plant’s life cycle from seed Effect of Plant‑Derived Smoke on Physiochemical
germination to vegetative and reproductive growth (Zhou Parameters Under Flooding Stress
et al. 2020). Flooding stress causes crops to grow under
hypoxic stress, which negatively mark all stages of plant Effects of Plant‑Derived Smoke on ATPase Abundance
development (Voesenek and Bailey-Serres, 2013). The and ATP Content Under Flooding Stress
growth and harvest of numerous crops is severely delayed
due to flooding stress (Komatsu et al. 2012). Many plants Flooding of plants results in a lower oxygen concentration in
under flood stress switch from aerobic respiration to fer- their surroundings, restricting their capacity for ATP produc-
mentation to accomplish their energy requirements (Bai- tion and energy transformation through mitochondrial oxi-
ley-Serres et al. 2012). These findings demonstrate that dative phosphorylation using oxygen (Banti et al. 2013). In
plant communities are under constant risk due to flooding order to cope with oxygen-poor conditions, plants generally
stress brought on by the ongoing climatic changes. activate anaerobic pathways to generate ATP, particularly
glycolysis, and regenerate ­NAD+ via ethanol fermentation
Journal of Plant Growth Regulation

to maintain glycolysis; this initial response includes the and ROS-scavenging compounds in plants (Sasidharan et al.
selective synthesis of flooding-inducible proteins involved 2018). Flooding stress activated ascorbate/glutathione cycle
in sucrose breakdown, glycolysis, and fermentation (Nishi- in soybean; additionally, it was further increased by the treat-
uchi et al. 2012). However, prolonged duration of waterlog- ment of plant-derived smoke (Otori et al. 2020). Ascorbate/
ging and anaerobic respiration ultimately leads to the accu- glutathione pathway is an important part of plant defence
mulation of toxic metabolites such as lactic acid, ethanol, system and helps to maintain a balance between the produc-
and aldehydes, combined with an increase in ROS notably tion and scavenging of ROS (Pang and Wang 2007). These
hydrogen peroxide, thus eventually leading to cell death results suggest that plant-derived smoke activates scaveng-
and plant senescence (Zhang et al. 2017). In soybean, ATP ing of ROS for rescuing soybean from flooding damage.
content decreased at the initial flooding stage (Nanjo et al.
2011; Yin et al. 2014). Comparative analysis of mitochon-
dria proteins indicated that proteins related to the electron Altered Metabolism of Sugars and Glycolysis are Associated
transport chain decreased in soybean because of flooding with Recovery of Smoke‑Treated Soybean After flooding
stress (Komatsu et al. 2011). On the other hand, Rehman Stress
et al. (2019) reported that plant-derived smoke solution
application up-regulated proteins related to carbohydrate Sucrose and starch molecules pass through enzymatic reac-
pathways were increased and glycolysis process might be tions to form glucose molecule in flooded and plant-derived
enhanced in the roots of chickpea leading to the production smoke-treated flooded soybean (Li et al. 2018). Flooded
of energy in the form of ATP. Flooding stress inhibited the and plant-derived smoke-treated flooded soybeans have dis-
respiratory chain and thus lower the production and abun- turbed sucrose/starch metabolism and glycolysis processes
dance of ATP in soybean root, however, plant-derived smoke (Li et al. 2018). Flooding stress and plant-derived smoke
treatment recovers soybean growth through increase of ATP in the presence of flooding activated sucrose synthase and
content by activation of ATPase (Otori et al. 2020). In nut- amylases enzymes in soybean to increase the conversion of
shell, flooding stress lowers the supply of oxygen and ATP starch and sucrose to glucose. Sucrose synthase and isoam-
contents but application of plant-derived smoke recovered ylase increase in smoke-treated flooded soybean; however,
plants from these drastic conditions. decrease beta-fructofuranosidase, which converts sucrose to
fructose. Plant-derived smoke treatment recovered soybean
Ascorbate/Glutathione Cycle is Activated with Treatment plant from flooding stress by changing sucrose/starch metab-
of Plant‑Derived Smoke Under Flooding Stress olism. Taken together, altered sucrose/starch metabolism of
plant-derived smoke-treated soybean might contribute to
ROS are enzymatic or non-enzymatic compounds syn- recovery after flooding stress.
thesized during metabolic pathways. Plant chloroplasts Regarding glycolysis, both treated soybeans had a higher
and mitochondria produced non-enzymatic ROS species amount of 6-phosphofructokinase-1, an essential enzyme
through electron transport chains. In both organelles, the that may redirect hexose phosphates to sugarcane's respira-
occasional leakage of electrons to oxygen during electron tory pathways (Wang et al. 2013). Phosphofructokinase is a
transport results in the partial reduction of oxygen, gener- vital enzyme in respiratory pathway which regulates soybean
ating superoxide, which subsequently gives rise to more flooding tolerance and growth attributes (Wang et al. 2017a,
ROS (Asada 2006). Plant-derived smoke increased ROS- b). Another glycolytic enzyme, glyceraldehyde-3-phosphate
scavenging proteins such as APX, glutathione reductase dehydrogenase, also strengthens soybean against abiotic
(GR), and POD as well as proteins related to mitochondrial stress (Hancock et al. 2005). Glyceraldehyde-3-phosphate
electron transport chain under flooding stress (Caverzan dehydrogenase interacts with phospholipase-D link with
et al. 2012). Plant-derived smoke activated ROS-scavenging cell membrane to transduce ROS hydrogen peroxide signal
compounds such as APX, GR, and POD against the produc- in Arabidopsis (Guo et al. (2012). It is believed that H­ 2S
tion of ROS in soybean root mitochondria under flooding increases the association of phospholipase-D and glyceral-
stress conditions. These ROS-scavenging compounds speed dehyde-3-phosphate dehydrogenases which might control
up the detoxification of different harmful ROS substances energy metabolism, growth control, and plant response to
(Caverzan et al. 2012). Low oxygen conditions resulted in ROS and water stress. This mechanism might also be acti-
synthesizing ROS which reduced or stopped electron trans- vated in soybean by flooding stress. The pyruvate kinase
port chain in the mitochondria (Chang et al. 2012). The sig- level was increased after flooding, which generated and con-
nalling of ROS via regulation of the production of ROS is served ATP for soybean survival and growth under flooding
considered an important component of hypoxia signalling stress. Plant-derived smoke treatment induced glycolysis,
and adaptive responses to flooding (Yamauchi et al. 2017). which helps in the recovery of soybean from flooding stress
An optimal plant growth required a balanced level of ROS (Li et al. 2018). These results suggest that plant-derived
 Journal of Plant Growth Regulation

smoke improves soybean recovery after flooding stress via smoke activated arginine metabolism which has the highest
a balance of sucrose/starch metabolism and glycolysis. nitrogen to carbon ratio and is considered as an essential
metabolite for many cellular and developmental processes
(Slocum 2005). Micallef and Shelp (1989) reported that
Mechanism of Alleviation of Flooding arginine accounted for 18% of the total protein nitrogen and
Through Plant‑Derived Smoke Solution is linearly accumulated throughout development in soybean
at Morphological Level cotyledon. Except for functioning as an amino acid for pro-
tein synthesis, arginine is a precursor for polyamines and
Proteins Increased in Soybean Cell Wall During NO (Winter et al. 2015). NO not only played role as a devel-
Recovery from flooding Stress opment regulator in promoting germination, leaf extension,
root growth, and fruit maturation (Neill et al. 2008) but also
The plant cell wall is a complex structure that fulfils a diverse a modulator of disease resistance which triggered hyper-
array of functions throughout the plant lifecycle (Houston sensitive cell death and activated the expression of several
et al. 2016). It provides mechanical support essential for defence genes (Romero-Puertas et al. 2004). These results
growth and development (Gigli-Bisceglia et al. 2020). Plants suggests that accumulation of arginine within soybean in
are exposed to various abiotic stresses during their entire response to plant-derived smoke might promote soybean
life (Shaik and Ramakrishna 2014), the cell wall acts as growth and development.
the first line of defense when the plant encounters environ- Plant-derived smoke enhanced ornithine synthesis via
mental stresses (Tucker and Koltunow 2014). Plant-derived alteration in arginine metabolism (Zhong et al. 2020). Orni-
smoke-treated soybean has higher number of proteins related thine has been confirmed as the key regulator of polyamine
to the cell wall than in flooded soybean (Li et al. 2018). biosynthesis and entire subset of pathways for glutamate
Beside this, the level of peptidyl-prolyl cis–trans isomerase to arginine (Majumdar and Minocha 2015). More impor-
was lesser in plant-derived smoke-treated flooded soybean tantly, it could also regulate putrescine metabolism, which
compared to flooded soybean (Li et al. 2018). Kuar et al. contributed to Gamma-aminobutyric acid (GABA) content
(2016) found that lower activity of peptidyl-prolyl cis–trans of the cells (Majumdar et al. 2013). GABA is a metabo-
isomerase activity plays a key role in stress tolerance. This lite with practical significance in plants. GABA accumu-
decrease in peptidyl-prolyl cis–trans isomerase in the smoke- lated in response to several abiotic or biotic stresses and
treated soybean cell wall indicates that plant-derived smoke was involved in interactions with varied pathways such as
promotes recovery after flooding stress (Li et al. 2018). It calcium-related pathway (Trobacher et al. 2013) and respira-
is believed that Bowman–Birk proteinase inhibitor plays a tory processes (Michaeli et al. 2011). The increase in the
key role in plant defence as their level elevated during abi- supply of carbon and reducing power from metabolism could
otic stress (Gitlin-Domagalska et al. 2020). Plant-derived be harnessed to engineer high level of phenylpropanoids in
smoke-treated soybean has lower Bowman–Birk proteinase tomato (Zhang et al. 2015). Similar metabolic alteration
isoinhibitor D-II than flooded cotyledon, hypocotyl, and root might exist in soybean treated with plant-derived smoke,
of soybean (Li et al. 2018). These results suggested that the since the increase of phenylpropanoids such as naringenin
accumulation of proteins related to the cell wall might play and piceatannol was observed (Zhong et al. 2020). These
an important role in soybean recovery after flooding stress. findings suggest that plant-derived smoke enhanced soy-
bean growth and accumulation of nutrient metabolites from
Plant‑Derived Smoke Regulated Ornithine‑Synthesis nitrogen fixation to carbon metabolism through ornithine-
Pathway in Soybean Under Normal Condition synthesis pathway.
and Encouraged Soybean Growth

Plant-derived smoke changed metabolic proteins in soybean. Conclusion and Future Prospective
Altered proteins were mainly related to protein synthesis and
degradation, especially, proteins related to amino acids such The positive role of plant-derived smoke in plant growth
as asparagine synthase, arginase, arginine succinate syn- regulation under normal conditions and abiotic stresses is
thase, serine carboxy-peptidase, and glutamine synthetase well proven. The role of plant-derived smoke solution in the
(Zhong et al. 2020). Amino acid analysis indicated that presence of salinity, heavy metal, temperature, and flooding
tyrosine, ornithine, and anserine significantly increased in stress are (i) plant-derived smoke solution may induce toler-
soybean treated with plant-derived smoke solutions. In addi- ance in plants against abiotic stresses through regulation of
tion, related metabolite such as urea, Gamma amino butyric the antioxidant system of plants; (ii) plant-derived smoke
acid (GABA), and succinic acid, along with NO content, solution may block the uptake of salt ions or heavy met-
increased as well. Based on KEGG database, plant-derived als solution through plant roots; (iii) plant-derived smoke
Journal of Plant Growth Regulation

alleviated flooding stress by activating cell wall proteins Ayala A, Munoz MF, Arguelles S (2014) Lipid peroxidation: pro-
and activated metabolic pathways; (iv) plant-derived smoke duction, metabolism, and signalling mechanisms of malondi-
aldehyde and 4-hydroxy-2-nonenal. Oxidat Med Cell Longev
solution suppressed stress-related genes in plant organ, and 2014:360438
thus increase tolerance in plants against stresses. It is con- Aydinalp C, Marinova S (2009) The effects of heavy metals on seed
cluded that plant-derived smoke is a potent abiotic stresses germination and plant growth on alfalfa plant (Medicago sativa).
alleviator and ameliorates the toxic effects of abiotic stresses Bulg J Agric Sci 15:347–350
Azam M (2016) Does environmental degradation shackle economic
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as a plant growth regulator and a stress alleviator. Sustain Energy Rev 65:175–182
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tive flooding survival strategies. Plant Physiol 160:1698–1709
Author Contributions SK contributed to the conception and design of Bandurska H (2022) Drought stress responses: coping strategy and
the manuscript. AK prepared figure and table. MMA wrote the first resistance. Plants 11(7):922
draft of the manuscript. SK commented on the previous versions of Banerjeea A, Tripathib DK, Roychoudhury A (2019) The karrikin ‘cal-
the manuscript. MJ and SUR read the manuscript. All authors read and isthenics’: can compounds derived from smoke help in stress
agreed the final manuscript. tolerance. Physiol Plant 165:290–302
Banti V, Giuntoli B, Gonzali S, Loreti E, Magneschi L, Novi G,
Paparelli E, Parlanti S, Pucciariello C, Santaniello A, Perata P
(2013) Low oxygen response mechanism in green organisms. Int
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