College of Horticulture and Forestry (Dr. Y.S. Parmar University of Horticulture and Forestry), Neri, Hamirpur, India
Correspondence
Meenakshi Thakur, College of Horticulture and Forestry (Dr. Y.S. Parmar University of Horticulture and Forestry), Neri, Hamirpur 177 001, Himachal Pradesh, India.
College of Horticulture and Forestry (Dr. Y.S. Parmar University of Horticulture and Forestry), Neri, Hamirpur, India
Correspondence
Meenakshi Thakur, College of Horticulture and Forestry (Dr. Y.S. Parmar University of Horticulture and Forestry), Neri, Hamirpur 177 001, Himachal Pradesh, India.
Hydrogen sulfide (H2S) is a small, reactive signaling molecule that is produced within chloroplasts of plant cells as an intermediate in the assimilatory sulfate reduction pathway by the enzyme sulfite reductase. In addition, H2S is also produced in cytosol and mitochondria by desulfhydration of l-cysteine catalyzed by l-cysteine desulfhydrase (DES1) in the cytosol and from β-cyanoalanine in mitochondria, in a reaction catalyzed by β-cyano-Ala synthase C1 (CAS-C1). H2S exerts its numerous biological functions by post-translational modification involving oxidation of cysteine residues (RSH) to persulfides (RSSH). At lower concentrations (10–1000 μmol L−1), H2S shows huge agricultural potential as it increases the germination rate, the size, fresh weight, and ultimately the crop yield. It is also involved in abiotic stress response against drought, salinity, high temperature, and heavy metals. H2S donor, for example, sodium hydrosulfide (NaHS), has been exogenously applied on plants by various researchers to provide drought stress tolerance. Exogenous application results in the accumulation of polyamines, sugars, glycine betaine, and enhancement of the antioxidant enzyme activities in response to drought-induced osmotic and oxidative stress, thus, providing stress adaptation to plants. At the biochemical level, administration of H2S donors reduces malondialdehyde content and lipoxygenase activity to maintain the cell integrity, causes abscisic acid-mediated stomatal closure to prevent water loss through transpiration, and accelerates the photosystem II repair cycle. Here, we review the crosstalk of H2S with secondary messengers and phytohormones towards the regulation of drought stress response and emphasize various approaches that can be addressed to strengthen research in this area.
1 INTRODUCTION
Drought-induced osmotic stress restricts the overall growth of plants due to the low rate of water absorption by roots and the high rate of transpiration (Blum, 1996). In addition to this, water deficiency leads to a significant reduction in leaf cell turgor, which ultimately causes a restriction in the expansion of cells, decreases leaf area, and rate of photosynthesis, thereby inhibiting the buildup of biomass (Chaves et al., 2003; Raja et al., 2020). Drought causes an imbalance between light capture and its utilization which results in the accumulation of reactive oxygen species (ROS) in the chloroplast, leading to disorganization of thylakoid membranes (Hussain et al., 2018; Kosar et al., 2020; Ladjal et al., 2000) and inactivation of photosystem II (PS II) by inhibition, both in the flow of electrons and electron transfer from the reduced plastoquinone (PQ) pool to the PS I reaction center (Dąbrowski et al., 2019; Giardi et al., 1996), as a consequence of oxidative stress. Net photosynthetic rate, chlorophyll fluorescence, and antioxidant activities in soybean were also influenced by water deficit (Iqbal et al., 2019). Several measures have evolved in plants to sustain photosynthetic activity by repairing PS II turnover (Giardi et al., 2013). Developing rice seedlings downsize their light-harvesting capacity to protect the chloroplasts from lipid peroxidation by ROS accumulation (Dalal & Tripathy, 2018). In semi-dwarf wheat varieties, semi-dwarfing genes result in reduced organ size and round leaf shape that contribute to improved drought tolerance through lower evaporation, and better preservation of cell membrane integrity (Petrov et al., 2018). Hussain et al. (2019) investigated the effect of drought stress in two maize hybrids, Xida 319 and Xida 889, and observed that Xida 889 exhibited greater drought tolerance due to a strong antioxidant defense system, higher osmolyte accumulation, and improved maintenance of photosynthetic pigments and nutrient balance. Besides the structural reorganization of the photosynthetic machinery many compounds, namely hydrogen peroxide (H2O2) (Niu & Liao, 2016), salicylic acid (Sohag et al., 2020), sodium metasilicate (Na2SiO3) (Parveen et al., 2019), nitric oxide (NO) (Montilla-Bascon et al., 2017), methylglyoxal (MG) lipid-derived signal molecules (monogalactosyldiacylglycerol and digalactosyldiacylglycerol) (Torres-Franklin et al., 2007), protein kinases (sucrose nonfermenting)-1-related protein kinases (SnRK) (Halford & Hey, 2009), mitogen-activated protein kinases (MAPKs) (Colcombet & Hirt, 2008) and H2S (Rajasheker et al., 2019; Santisree et al., 2019) have emerged to play a protective role in drought tolerance. Li et al. (2015) suggested that exogenous application of H2S in wheat under drought stress decreased the production of ROS through an increase in the activities of antioxidant enzymes superoxide dismutase (SOD) and catalase (CAT), thus, reducing the oxidative damage of PS II and facilitating its repair through enhancement of phosphorylation, degradation, and synthesis of the D1 protein. Chen et al. (2016) reported that exogenous application of H2S increased both the water- and osmotic-potential of Spinacia oleracea leaves under drought stress by reducing malondialdehyde (MDA) and upregulating the genes related to the biosynthesis of polyamines (PAs) and sugars.
H2S is known to play a vital role in the regulation of plant physiological processes (Hancock, 2019; Olas, 2014). H2S at low concentrations regulates seed germination (Baudouin et al., 2016; Li, 2020), root growth (Hu et al., 2020), stomatal apertures (Lisjak et al., 2011; Liu, Wang, et al. 2021), flower senescence (Huo et al., 2018), photosynthesis (Chen et al., 2011), autophagy (Alvarez, Garcia, Moreno, et al., 2012; Laureano-Marin et al., 2016; Romero et al., 2014), and biotic and abiotic stress tolerance (Hancock & Whiteman, 2014; Kaya, Ashraf, et al., 2020; Kaya, Higgs, et al., 2020; Li, 2013; Shi et al., 2015; Zulfiqar & Hancock, 2020). This molecule has been known to alleviate various abiotic stresses, for example, heavy metal (Ahmad et al., 2020; Fang et al., 2016; Li, Shah, et al., 2021; Li, Wang, & Shen, 2012; Luo et al., 2020; Ozfidan-Konakci et al., 2020; Shen et al., 2013; Zhang, Hu, et al., 2008), drought (Shen et al., 2013), water logging (Xiao et al., 2020), high temperature (Li, Gong, et al., 2012), low temperature (Liu et al., 2020; Nasibi et al., 2020; Tang et al., 2020) salinity (Ding et al., 2019; Ma et al., 2018; Shi et al., 2013; Yastreb, et al. 2020), and alkalinity (Bahmanbiglo & Eshghi, 2021; Dawood et al., 2021). It is produced endogenously within plants, suggesting its role as a signaling molecule (Fuentes-Lara et al., 2019; Li, 2013; Zhang et al., 2021). Also, exogenous application of H2S leads to increased cysteine production, which is important for the biosynthesis of proteins and other important cellular components essential for normal growth and development. H2S exposure also enhances the accessibility of reduced form of sulfur for glutathione synthesis, which has a dominant role in the defense responses against various stresses by scavenging ROS (Calderwood & Kopriva, 2014). This review aims to provide a comprehensive update on the different routes of biosynthesis of H2S in plants and its crosstalk with secondary messengers and phytohormones during the drought stress response. We conclude the review by suggesting possible research gaps that need to be systematically addressed to map the various components of signaling pathways of H2S-mediated drought tolerance.
2 H2S AS A SIGNALING MOLECULE
The first study on the positive effects of H2S was conducted in the 1960s, indicating that H2S affects the vegetative growth of plants as well as provides resistance against nematodes (Calderwood & Kopriva, 2014; Rodriguez-Kabana et al., 1965). At high concentrations (˃1000 μmol L−1) H2S acts as a phytotoxin due to its inhibitory action on mitochondrial cytochrome c oxidase (Koch & Erskine, 2001). At high concentrations, it becomes highly deleterious if combined with abiotic stresses viz., high temperature, drought, or salinity (Lisjak et al., 2013). However, at lower concentrations (10–1000 μmol L−1) it is involved in signaling in combination with other small reactive molecules such as H2O2, NO, and carbon monoxide (CO) (Caverzan et al., 2021; Hancock 2019; Lisjak et al., 2013; Olson, 2009).
The signaling property of H2S may be attributed to its ability to interact with thiol (−SH) groups of cysteine residues of proteins via post-translational modification (PTM) such as persulfidation (Aroca et al., 2018; Corpas et al., 2019; Li et al., 2020; Liu Q, Zhou, et al., 2021). Protein persulfidation involves a redox modification that controls various physiological processes in plants (Aroca et al., 2020; Filipovic & Jovanovic, 2017; Gotor et al., 2019). Persulfidation regulates protein activities by various mechanisms that involve changes in their subcellular localization, biochemical activity, protein–protein interactions, conformation as well as stability (Aroca et al., 2017; Filipovic et al., 2018). Persulfide modification increases the expression of H2S-producing enzymes. Protein thiol-groups play a crucial role in regulating numerous interactions which can cause activation or inhibition of the function of targeted proteins (Bhatnagar & Bandyopadhyay, 2018; Duan et al., 2017). During PTMs, H2S competes with other molecules like cyanide (CN−), NO, glutathione (GSH), and fatty acids that create different modifications such as S-cyanylation (Garcia et al., 2019), S-nitrosation (Corpas et al., 2019), S-glutathionylation (Diaz-Vivancos et al., 2015), and S-acylation (Zheng et al., 2019), respectively (Figure 1).The direct modification of H2S-mediated cysteine residues is not possible, an additional step involving oxidation is required (Cuevasanta et al., 2015). On being encountered by oxidative stress, irreversible oxidative modification of thiol (−SH) groups of cysteine residues results in the production of sulfenic acids (−SOH) which, if the stress persists can be further oxidized to form sulfinic (−SO2H), and sulfonic (−SO3H) acids. If sulfenic acid is buried deep into the protein pockets, it cannot easily be accessible and reduction takes place to form thiols. Sulfenic acid reacts with H2S almost 600 times faster than glutathione (Cuevasanta et al., 2015). Oxidative stress involving excessive production of H2O2 results in enhanced persulfidation (Wedmann et al., 2016). Persulfidation is the simplest way to protect proteins from oxidative damage, hence, it can be speculated that it is an evolutionary trace from the period when life arose in a sulfide-rich environment. Persulfides act as good scavengers of ROS, if the stress persists, leading to the formation of perthiosulfonic (−SSO3H), which can easily be reduced by thioredoxin (Trx) for the restoration of free thiols, thus, recycling the bound H2S (Figure 2) (Filipovic, 2015; Wedmann et al., 2016). This hypothesis is justified by the experiments on the exogenous treatment of H2S to alleviate abiotic stress response (Zhang, Hu, et al., 2008). An enormous amount of persulfidated proteins are present in the chloroplasts of plant cells that suggest the formation of H2S by sulfur assimilation process along with the considerable amount of ROS.
Proposed model for protein thiol (−SH) modifications through the incorporation of (A) H2S (persulfidation), (B) cyanide (S-cyanylation), (C) NO (S-nitrosation), (D) glutathione (GSH) (S-glutathionylation), (E) fatty acid (S-acylation)
A model depicting the complicated interactions between signaling molecule H2S and reactive oxygen species (e.g. H2O2). (A) Drought stress can result in the accumulation of ROS (•O2 and H2O2) as well as H2S, which is responsible for altering the activities of antioxidant enzymes viz., CAT, APX, DHAR, and GR by using associated reducing substrates such as ascorbate (ASC), glutathione (GSH), and NADPH to reduce ROS by metabolizing H2O2. (B) On exposure to oxidative stress, ROS reversibly oxidize thiol (−SH) groups of cysteine residues present in the proteins to sulfenic acids (−SOH). The excessive oxidants can further cause irreversible hyperoxidation of sulfenic acid (−SOH) to form sulfinic (−SO2H) or sulfonic (−SO3H) acids. H2S on reaction with sulfenic acid residues results in the formation of persulfidated (−SSH) proteins. Persulfidated proteins either reduce back to thiol by the action of thioredoxin (Trx) or can react with H2O2 to form perthiosulfenic (−SSOH), perthiosulfinic (−SSO2H), and perthiosulfonic (−SSO3H) acids which again can be restored back to thiol by thioredoxin. Additionally, H2S maintains protein stability by degrading these oxidized proteins, thus negatively controlling the autophagic pathway. This dual role of H2S can support plants to form proteins that are functionally active against oxidative stress as well as to lower down the consumption of energy by de novo synthesis of protein for growth, development, and defense response against abiotic stress (modified from Chen, Tian, et al., 2020)
3 AVAILABILITY OF H2S TO PLANT CELLS
Plants may respond to H2S obtained from two sources, that is, from the environment (extracellular) or from within cells (intracellular).
3.1 Extracellular sources
There are numerous environmental sources of H2S, ranging between natural and artificial or man-made. Natural sources of H2S include the coastal marine sediments (Hansen et al., 1978) or anoxic soils found in marshland (Morse et al., 1987) or volcanic eruption (Aiuppa et al., 2005). Man-made sources include the release of H2S from geothermal industries (Bacci et al., 2000), agricultural activities (Aneja et al., 2008), waste treatment plants (Zhang, De Schryver, et al., 2008), and cars with catalytic converters (Kourtidis et al., 2008). External sources are mainly responsible for the phytotoxic effect on plants due to the higher concentrations in which they are released. A recent study has reported that sulfur dioxide (SO2) which acts as a common air pollutant, at low concentration (10 mg m−3) triggered the accumulation of H2S in wheat seedlings to enhance drought stress tolerance (Li, Yi et al., 2021). SO2 on entering into plants through stomata, forms SO32− which can be reduced to H2S by sulfite reductase, thereby suggesting a complex interplay of SO2 and H2S in plants (Li & Yi, 2012).
3.2 Intracellular sources
Intracellular sources of H2S in plant cells are cytosol, mitochondria, and chloroplast (Figure 3). In the cytosol, the majority of H2S is formed by the desulfhydration of l-Cys along with pyruvate, and ammonia as byproducts in a reaction catalyzed by the enzyme l-Cys desulfhydrase (DES1) (Alvarez et al., 2010; Alvarez, Garcia, Moreno, et al., 2012; Gotor et al., 2010; Riemenschneider, Nikiforova, et al., 2005; Riemenschneider, Wegele, et al., 2005). This enzyme has been characterized in plastids of Arabidopsis thaliana (Alvarez et al., 2010). A similar enzyme, that is, d-cysteine desulfhydrase (DCD1) which decomposes d-Cys into pyruvate, H2S, and NH3 has also been reported in the mitochondria (Riemenschneider, Wegele, et al., 2005). DCD1 (Riemenschneider, Wegele, et al., 2005) and nitrogen fixation homologs 1 and 2 (NSF1 and NFS2) (Heidenreich et al., 2005) have also been reported to produce H2S in the cytosol. In chloroplast, H2S is produced as an intermediate of the sulfur assimilation pathway. The concentration of H2S is higher in chloroplasts (125 μM) as compared to the cytosol (55 μM) (Krueger et al., 2009). However, within organelles, H2S is present in its ionized form due to the alkaline pH and is thus unable to pass through the membranes towards the cytosol (Kabil & Banerjee, 2010). It plays an important role in the chloroplasts where it can act as a signaling molecule and regulate cellular metabolism, however, in mitochondria it acts as a potent toxin that mainly targets respiration (Birke et al., 2015).
Schematic illustration of the key pathways involved in H2S biosynthesis. The dotted arrow indicates that chloroplast, cytosol, and mitochondria are involved in a reverse reaction between acetate and l-cysteine to synthesize O-acetyl-l-serine and liberate H2S
In mitochondria, H2S is produced during cyanide metabolism catalyzed by β-cyano-Ala synthase C1 (CAS-C1) (Alvarez, Garcia, Romero, & Gotor, 2012; Garcia et al., 2010; Yamaguchi et al., 2000). The turnover of iron–sulfur clusters and detoxification of mitochondrial cyanide requires the catabolism of cysteine releasing sulfide (Garcia et al., 2010). Detoxification mechanisms regulate the formation of sulfide during sulfur assimilation and/or cynaide metabolism as its accumulation is lethal for the plants. An important detoxification mechanism involves the fixation of sulfide into cysteine under severe sulfide levels (Youssefian et al., 1993).
The detailed pathway for the production of H2S via the sulfur assimilation pathway in chloroplasts is represented in Figure 4. Plants take up sulfate (SO42−) from the soil or atmosphere. Following this, activation of sulfate takes place to form adenosine 5′-phosphosulfate (APS) by adenylation utilizing the energy of ATP hydrolysis catalyzed by ATP sulfurylase (ATPS). In plastids, activated sulfate, that is, APS is reduced to sulfite by the enzyme APS reductase (APR). Ferredoxin dependent sulfite reductase (SiR) further reduce sulfite to sulfide (Garcia et al., 2015), followed by its incorporation to O-acetylserine (OAS) to form cysteine which acts as a precursor of all organic compounds containing sulfur in reduced form in plants or animals, for example, proteins, cofactors, vitamins, and glutathione (Takahashi et al., 2011). The sulfur assimilation pathway that involves the reduction of sulfate to form sulfide followed by integration of sulfide into OAS is the first step for entry of reduced sulfur into the plant metabolism and plays a crucial role in growth and development (Birke et al., 2013). OAS is provided to the pathway through the reaction catalyzed by serine acetyltransferase (SAT). A complex called cysteine synthase complex (CSC) is formed by the interaction of SAT and O-acetylserine (thiol) lyase (OAS-TL) and is involved in demand-driven regulation of cysteine synthesis (Feldman-Salit et al., 2012; Wirtz et al., 2010). The next step involves the dissociation of OAS from CSC, and the complex is stabilized by sulfide. For cysteine synthesis, SAT is the rate-limiting enzyme and cysteine acts as its strong feedback inhibitor. However, upon the formation of the CSC complex, the sensitivity of SAT for feedback inhibition is decreased strongly, which promotes the enzyme activity and formation of OAS. As a result, there is an enhancement in the OAS-TL-catalyzed turnover of reduced sulfur into cysteine (Feldman-Salit et al., 2009; Wirtz et al., 2010). Further cysteine is converted to H2S by the action of the enzymes DES1 and DCD1.
OAS and cysteine synthesis take place in cytosol, chloroplasts, and mitochondria due to the presence of isoforms of SAT and OAS-TL in all three compartments. SAT5 and OAS-TL A are present in cytosol, SAT1 and OAS-TL B in chloroplasts, and SAT3 and OAS-TL C in mitochondria (Birke et al., 2013; Watanabe et al., 2008). Reverse genetics studies have suggested that a certain redundancy exists between the three isoforms of SAT and OAS-TL, indicating exchange of sulfide, OAS, and cysteine among these three cell compartments (Lee et al., 2014; Watanabe et al., 2008) (Figure 5). These isoforms possess specific roles in different compartments as OAS-TL C is an important regulator of the activity of SAT3 in mitochondria that provides the massive amount of OAS, whereas OAS-TL A within cytosol plays a vital role in the synthesis of cysteine (Birke et al., 2013; Haas et al., 2008; Wirtz et al., 2012).
Pathways of assimilatory sulfate reduction in plants. The activated sulfate, that is, APS acts as a branching point between primary and secondary metabolism of sulfur because either it can be phosphorylated by APS kinase (APK) to form 3′-phosphoadenosine 5′-phosphosulfate (PAPS), which acts as a donor of activated sulfate and results in the formation of secondary metabolites, such as glucosinolates (GLS) or can lead to the OAS-TL-mediated production of H2S (modified from Calderwood & Kopriva, 2014)
4 H2S MEDIATE SIGNALING IN PLANTS IN RESPONSE TO DROUGHT STRESS
Drought stress exerts several deleterious effects on plants involving osmotic stress, oxidative stress, damage to PS II, loss of cell integrity, and so on, which affects their normal growth and development. H2S acts as a signaling molecule that causes a number of adaptations in the plant cells in response to drought stress, which is discussed below.
4.1 Accumulation of osmoprotectants
During drought-induced water deficit and osmotic stress, the tolerance in plants may be provided by the buildup of compatible low-molecular-weight osmoprotectants like soluble sugars, sugar alcohols, proline, and glycine betaine (GB) (Garcia-Mata & Lamattina, 2001; Rivero et al., 2014). According to Rivero et al. (2014), these osmoprotectants can vary significantly in their composition as well as content depending upon the species and environmental conditions. Besides these molecules, polyamines (PAs), including putrescine, spermidine, and spermine are biological organic-amines that are involved in plant growth as well as stress tolerance (Takahashi & Kakehi, 2010). Mohammadi et al. (2018) reported that exogenous application of putrescine (20 mg L−1) improved leaf water content, essential oil content, accumulated dry matter, reduced cell injury indices, and upregulated antioxidant enzyme activities in Thymus vulgaris under drought stress conditions. In plants, PAs increase considerably on exposure to abiotic stresses like heat, chilling, salinity, or drought (Takahashi & Kakehi, 2010; Tiburcio et al., 2014). The metabolic pathway of polyamines involves nitrogen or carbon metabolism along with crosstalk with other stress-protective metabolites such as signaling molecules and phytohormones (Moschou et al., 2012; Tiburcio et al., 2014). The over-expression of genes related to PA biosynthesis resulted in enhanced PA content and improvement in drought stress tolerance (Alcazar et al., 2010; Capell et al., 2004). Kasinathan and Wingler (2004) observed that knockout/knockdown mutants with abolished or limited capacity to synthesize PAs were more susceptible to drought stress as compared to wild-type plants. Li et al. (2019) reported that spermidine activated L/D-cysteine desulfhydrase (L/DCD) pathway of H2S signaling in white clover under dehydration stress.
Chen et al. (2016) proposed a model to depict the role of H2S in regulating drought stress tolerance by involving the biosynthesis of polyamines and sugars. Spinacia oleracea seedlings exposed to drought stress were treated with exogenous H2S donor (NaHS) and upregulation in the expression of genes for PA biosynthesis, that is, ornithine decarboxylase (ODC), N-carbamoylputrescine amidohydrolase (CPA), and arginine decarboxylase (ADC), and downregulation in the expression of S-adenosyl-Met-decarboxylase (SAMDC) were observed resulting in elevated polyamine levels. The expression of genes related to sugar biosynthesis was also studied and it was noticed that sugar biosynthetic genes encoding fructose-1,6-bisphosphatase (FBPase), trehalose-6-phosphate synthase (T6PS), and sucrose phosphate synthase (SPS1) were upregulated resulting in enhanced fructose and trehalose contents; and reduced glucose and sucrose contents in plant tissues (Figure 6).
Pathway for H2S-mediated biosynthesis of polyamines and sugars during drought exposure in plants (modified from Chen et al., 2016)
The exogenous application of NaHS (H2S donor) or up-regulation of H2S biosynthesis genes such as L/DCD under normal growth conditions triggers H2S signaling. On application in plant tissues, NaHS is dissociated to Na+ and HS− in the solution followed by association of HS− with H+ to form H2S (Hosoki et al., 1997). NaHS releases H2S with an instant burst which soon dissipates, whereas morpholin-4-ium 4-methoxyphenyl (morpholino) phosphinodithionate (GYY 4137) another donor of H2S, releases H2S much more slowly and in a manner that is more likely to reflect the physiological generation of H2S (Lisjak et al., 2011). Lisjak et al. (2011) applied NaHS and GYY 4137 to Capsicum annuum and observed that the GYY 4137 resulted in delayed release of H2S than NaHS. H2S can easily penetrate the plant cells and due to its high lipophilic property can be followed from one tissue to the other resulting in the regulation of physiological processes. This was confirmed by treating strawberry seedlings with NaHS (0.1 mM) resulting in a significantly high concentration of H2S, that is, 35 nmol g−1 FW in leaves as compared to untreated control plants, that is, 25 nmol g−1 FW (Christou et al., 2013). Zhang, Dou, et al. (2010) reported that NaHS-treated wheat seeds had 4.5 μmol g−1 dry weight (DW) of the endogenous level of H2S which was slightly higher than that of untreated seeds (1.7 mol g−1 DW). Various researchers have reported that H2S can significantly develop drought stress tolerance in different plant species (Table 1). H2S provides tolerance against drought-induced oxidative and osmotic damage by regulating the energy production leading to delayed leaf senescence, enhancing the antioxidant enzyme activities, reducing transpiration rate by regulating stomatal conductance, regulating the expression of genes for drought stress tolerance such as DREB and RD29A, or by accumulating osmoprotectants such as soluble sugars, sugar alcohols, glycine betaine, and proline (Chen et al., 2016; Jin et al., 2011; Jin et al., 2018).
Table 1.
The physiological and biochemical effects of the exogenous application of H2S donor on plants exposed to drought stress
Plant species
H2S donor
Main effect
Reference
Arabidopsis thaliana
GYY 4137/
NaHS (80 μM)
Stomatal closure; enhanced H2S synthesis and increased survival rate
Higher survival of seedlings; significant decrease in the size of stomatal aperture; increased expression of drought associated genes such as DREB2A, DREB2B, CBF4, and RD29A
Diminished drought induced oxidative damage due to increased accumulation of secondary metabolites, strengthened antioxidant capacity and maintenance of ion homeostasis
Increased water and osmotic potential of leaves; reduced MDA; increased levels of soluble sugars and PAs; upregulation of genes such as choline monooxygenase (SoCMO), betaine aldehyde dehydrogenase (SoBADH), aquaporin (SoPIP1;2) as well as genes related to the biosynthesis of PAs and soluble sugars
Increased activities of ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase, and γ-glutamylcysteine synthetase; higher contents of reduced ascorbic acid, reduced glutathione, total ascorbate, and total glutathione
Reduction in oxidative stress by enhanced activities of SOD and CAT; acceleration of PS II repair cycle; increased turnover of D1 protein by enhancing D1 protein phosphorylation, degradation, and synthesis
Induction of “ribosome biogenesis in eukaryotes,” “protein processing in endoplasmic reticulum,” “fatty acid degradation” and “cyanoamino acid metabolism” under drought stress
Decreased accumulation of H2O2 and malondialdehyde in leaves; increased activities of SOD, CAT, and POD; elevated concentration of proline, anthocyanins, and flavonoids
The physiological and biochemical effects of H2S from various studies as compiled in Table 1 are summarized diagrammatically in Figure 7 for the ease of comprehension. Drought-induced osmotic and oxidative stress can be inhibited by the exogenous application of NaHS. Drought stress destroys cell integrity, damages PS II, and causes water deficit within plant cells. Exogenous NAHS application reduces the content of MDA, lowers lipoxygenase activity to maintain the cell integrity; causes ABA-mediated stomatal closure to prevent water loss through transpiration and increases the turnover of D1 protein, and accelerates PS II repair cycle. These changes are brought about by H2S-mediated accumulation of PAs, soluble sugars, GB, and an increase in the activities of antioxidant enzymes, such as SOD, CAT, peroxidase (POD), and so on, those provide drought stress adaptation to the plants. The signaling role of H2S in abiotic stress tolerance is through upregulation of the antioxidant defense system that is primarily responsible for maintaining homeostasis in the stressed plants.
Cellular response in plants on exogenous application of H2S donor (NaHS) under drought stress
5 H2S CROSSTALK WITH OTHER SIGNALING COMPOUNDS
H2S interacts with secondary messengers (NO, H2O2, Ca2+, polyamines) and plant hormones (ABA, gibberellic acid, ethylene) that play a vital role in plant growth and development by regulating a range of physiological processes and imparting abiotic stress tolerance (Arif et al., 2021; Corpas, 2019; He et al., 2019; Huang et al., 2021; Li, Xiang, et al., 2021; Shivaraj et al., 2020). In addition to this, H2S also acts as a potent signal molecule in plant cross-adaptation that might induce resistance to other abiotic stresses such as heavy metal, salt, cold, heat, flooding, and so on (Li et al., 2016; Pandey & Gautam, 2020). In spinach plants, H2S treatment induced drought tolerance by increasing proline content and by stimulating polyamine biosynthesis (Chen et al., 2016). Garcia-Mata and Lamattina (2010) observed that H2S crosstalk with ABA to induce stomatal closure in A. thaliana and Vicia faba. Stomatal closure reduced transpiration and further allowed H2S to rapidly enter into mitochondria and chloroplast stroma to reduce the excessive production of ROS due to abiotic stress response (Jin et al., 2013). Drought stress experiments on wheat showed that ABA biosynthesis as well as signaling is induced by H2S (Ma et al., 2016). It was observed that NaHS application in wheat seedlings under drought stress increased the plant height, leaf relative water content, and activities of antioxidant enzymes. Pretreatment with NaHS resulted in reduced MDA and H2O2 contents in both leaves and roots. In leaves, there was an upregulation of the expression of genes encoding for ABA biosynthesis and its reactivation; whereas in roots, there was an upregulation of the expression of genes encoding for ABA biosynthesis and its catabolism implying that exogenous application of H2S leads to ABA signaling that ultimately participates in drought stress tolerance in wheat plants. It was also observed that H2S mediates ABA signaling via an ABA receptor as in response to NaHS pretreatment under drought stress, there was an upregulation of the transcription levels of genes encoding ABA receptors (TaRCAR and TaCHLH) in leaves and roots. The crosstalk between H2S and ABA helps in imparting drought stress tolerance to wheat plants.
Several studies have reported that H2S produced by DES1 catalyzed pathway plays an important role in drought stress tolerance through ABA signaling in guard cells (Du et al., 2019; Garcia-Mata & Lamattina, 2010; Jin et al., 2013; Zhang et al., 2020). The enzyme DES1 is required in ABA-dependent stomatal closure as well as in ABA-mediated signal transduction pathways (Scuffi et al., 2014; Zhang et al., 2019). Pandey (2014) observed that in des1 knockout mutants, the stomata fail to close even in response to ABA unless an exogenous H2S donor is provided.
Besides its interaction with ABA (Scuffi et al., 2014), H2S also interacts with gibberellic acid (Banerjee et al., 2018; Xie et al., 2014), ethylene (Liu et al., 2011; Liu et al., 2012), H2O2 (Liu & Xue, 2021; Zhang, Dou, et al., 2010) and NO (Bhuyan et al., 2020; Hasanuzzaman et al., 2020; Lisjak et al., 2011; Paul & Roychoudhury, 2020; Singh et al., 2020) to modify their signal. In guard cell signaling, it has been noticed that H2S increased the formation of NADPH oxidase-dependent H2O2 and phospholipase d-derived phosphatidic acid. H2S acts upstream of NADPH oxidase in ABA-induced stomatal closure as the induction of stomatal closure by sulfurating molecules is impaired in rbohD and rbohF mutants (unable to encode respiratory burst oxidase homolog proteins D and F) (Scuffi et al., 2018). H2S promotes NO production and acts upstream of NO to modulate ABA-dependent stomatal closure (Scuffi et al., 2014; Chen, Jia, et al., 2020; Chen, Tian, et al., 2020). Shan et al. (2020) reported that H2S interacts with NO to regulate the ascorbate-glutathione cycle in wheat seedlings during water stress. The interaction of H2S with NO induced the activities of H2S-synthesizing enzymes (L/DCD) to activate the defense system of wheat seedlings against osmotic stress (Khan et al., 2017). NO results in stomatal closure as the lack of endogenous NO significantly reduced the H2S-mediated stomatal closure. Jin et al. (2013) reported that H2S regulates the expression of ion-channel genes, and may act as a signaling molecule in stomatal movements which are regulated by ion channels. The stomatal movement is regulated by turgor pressure, which depends upon the concentrations of K+ and anions in guard cells. To study the effects of H2S on ion channels, the expression levels of genes encoding channel-protein were compared among the lcd mutant (l-cysteine desulfhydrase mutant) and the wild type. In the lcd mutant, the expression of genes encoding Ca2+ and outward-rectifying K+out channels was decreased, whereas inward-rectifying K+in and anion channels was increased. Thus, the lack of H2S in the lcd mutant changed the expression of genes encoding an ion-channel protein, which may lead to variation in the concentration of ions in guard cells and cause stomatal movement. Xuan et al. (2020) suggested that H2S may cooperate with ABA signaling to enhance the drought stress tolerance in plants by activating Ca2+ signaling and inward-rectifying K+ channels.
To sum up, the literature suggests a strong relation between H2S and drought tolerance which is controlled through its interaction with various hormones and secondary messengers that modifies the molecular network of the cell.
6 CONCLUSIONS AND FUTURE PERSPECTIVES
H2S acts as a signaling molecule at low concentrations to regulate a myriad of plant physiological processes like seed germination, development of roots, stomatal apertures, flower senescence, and pathogen attack. It also plays an important role in abiotic stress adaptation in plants against heavy metal exposure, high temperature, salinity, and drought. However, a comprehensive picture of the action of H2S under abiotic stresses needs to be investigated at various developmental stages. Exogenous application of H2S donors such as NAHS/GYY 4137 reduce oxidative stress by various mechanisms, that is, (1) scavenging of ROS and lowering lipoxygenase activity to maintain the cell integrity, (2) causing ABA-mediated stomatal closure to prevent water loss through transpiration, (3) increasing turnover of D1 protein and accelerating PS II repair cycle, and (4) accumulating compatible solutes like polyamines, soluble sugars, glycine betaine, and increase in the activities of antioxidant enzymes (Figure 8). The signaling property of H2S is attributed to its ability to interact with thiol groups of cysteine residues of proteins via post-translational modification, that is, persulfidation. Intracellular sources of H2S are cytosol, mitochondria, and chloroplast, however, the majority of H2S is produced in the cytosol of the plant cells by the desulfhydration of l-cysteine along with pyruvate, and ammonia as byproducts in a reaction catalyzed by the enzyme l-cysteine desulfhydrase. Nonetheless, an extensive review of the literature reveals that the regulation of H2S production and its target sites in the various organelles is poorly characterized. The use of pharmacological approaches for the identification of precise enzyme inhibitors of H2S biosynthetic pathway can help in a better understanding of the intracellular H2S production. Microbes possessing l-cysteine desulfhydrase activity for the production of H2S can be used as models for defining the physiological function of H2S under drought stress.
Summary of the physiological and biochemical changes mediated by H2S to counteract the adverse effects of drought stress
H2S is also involved in crosstalk with NO, H2O2, Ca2+, ABA, GA, ethylene, and polyamines that play a vital role in drought stress response in plants. However, there is still a need to elucidate the complexity by which H2S and other signaling molecules interact with each other to reveal the status of H2S with other molecules involved in signal transduction networks in plants. With the increasing sophistication of the analytical tools, the receptors for H2S can be identified at the cellular level. Like other plant signaling molecules, the role of transcription factors and protein kinases in the H2S-regulated signaling cascades under drought stress can be examined. Therefore, in future research, there must be a priority for the development of a highly efficient method for detection of H2S by utilizing various omics-mediated approaches to screen out H2S-related locus on a large scale. The current understanding of the crucial role of H2S in imparting drought stress tolerance is obscure and needs to be strengthened by using mutants to unravel the biochemical pathways that are altered in response to H2S under drought stress. The gene modification tools can explain the importance of H2S in drought tolerance at the theoretical level of understanding which can be further extrapolated for agronomic benefits in the crop plants facing drought threat.
AUTHOR CONTRIBUTIONS
Meenakshi Thakur and Anjali Anand conceived and outlined the review. Meenakshi Thakur wrote the manuscript. Anjali Anand reviewed and edited the manuscript.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
Data sharing is not applicable to this article as no new data were created or analyzed in this study.
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