УДК 581.1

Hydrogen sulfide: a multifunctional gaseous molecule in plants1

© 2013 Z. G. Li

School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, P.R. China

Received October 12, 2012

Hydrogen sulfide (H2S), a gaseous transmitter, has long been considered as a phytotoxin, but nowadays as a small molecule with multiple functions fulfilled at low concentrations. H2S has many positive effects on plant growth, development, and the acquisition of plant stress tolerance. The focus of this review is to summarize the generation and properties of hydrogen sulfide and its potential physiological functions, including mediating stomatal movements; mediating the responses to abiotic stressors, such as heavy metals, salt, drought and heating; involving in organogenesis and growth; regulating senescence; priming seed germination; and enhancing photosynthesis. Future prospects are also presented.

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1 This text was submitted by the authors in English.

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Abbreviations: AOA  aminooxyacetic acid; APR  adenosine-5-phosphosulphate reductase; APX  ascorbate peroxidase; CaM  calmodulin; CAT  catalase; CPZ  chlorpromazine; DPI  diphenylene iodonium; GYY4137  p-(methoxyphenyl)morpholino-phosphine-dithionic acid; HM  heavy metals; HO-1/CO  haem oxygenase-1/carbon monoxide; L-/D-CD  L-/D-cysteine desulfhydrase; LSCM  laser scanning confocal microscopy; MS  3-mercaptopyruvate sulfurtransferase; NOX  NADPH oxidase; OAS-TL  O-acetyl-L-serine (thiol) lyase; P5CS  Δ1-pyrroline-5-carboxylate synthetase; PME  pectin methylesterase; POD  guaiacol peroxidase; ppb  parts per billion; ProDH  proline dehydrogenase; RWC  relative water content; SHAM  salicylhydroxamic acid; SNP  sodium nitroprusside; SOD  superoxide dismutase; TFP  trifluoperazine; RBCL  Rubisco large subunit; RBCS  Rubisco small subunit; RR  ruthenium red; Rubisco  ribulose-1,5-bisphosphate carboxylase.

Corresponding author: Li Zhong-Guang. School of Life Sciences, Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Province, Yunnan Normal University, Kunming, 650092 P.R. China. Fax: 871-594-1365; e-mail: zhongguang_li@163.com

 Keywords: plants  abiotic stress  hydrogen sulfide  signaling molecule  stress tolerance

 

INTRODUCTION

Hydrogen sulfide (H2S), colorless and flammable gas, has long been considered as a phytotoxin, which is harmful to plant growth and development, but nowadays as a small molecule with multiple functions fulfilled in plants at low concentrations [1]. In many plant species, such as alfalfa, grape, or lettuce, fumigation with H2S caused lesions on leaves, defoliation, and reduced plant growth [1]. It was also found repeatedly that H2S inhibited oxygen release from young seedlings of six rice cultivars and suppressed the uptake of nutrients, such as phosphorus [1, 2]; these results support the role of H2S as a phytotoxin. In contrast, the lower levels of fumigation, 100 parts per billion (ppb), caused a substantial increase in the growth of alfalfa, lettuce, and sugar beet; it was also noted that in some rice cultivars H2S could promote nutrient uptake [1].

Increasing evidence illustrates that H2S acts as an important signaling molecule to regulate many physiological processes in animal systems [1]. In plant systems, a lot of physiological functions of H2S have been found. Lisjak et al. [3] reported that H2S caused stomatal opening in the light and prevented stomatal closure in the dark by reducing the accumulation of NO in Arabidopsis thaliana, while drought stress led to stomatal closure through the increase in the content of H2S due to the enhanced expression and activity of D-/L-cysteine desulfhydrase (L-/D-CD), a key enzyme of H2S biosynthesis in leaves of Vicia faba [4]. Our previous results also found that H2S was a mediator in H2O2-induced seed germination of Jatropha curcas [5], and NaHS pretreatment significantly increased a survival percentage of maize seedlings and tobacco suspension cultured cells under heat stress and regrowth ability after heat stress by alleviating a decrease in the vitality of cells and accumulation of MDA [6, 7].

For excellent additional knowledge, I refer readers to wonderful review written more recently [1]. The focus of this review is to summarize current knowledge about H2S generation and properties and its potential physiological functions, including mediating stomatal closure; mediating the responses to abiotic stressors, such as heavy metals, salt, drought, and heating; involving in organogenesis and growth; regulating senescence; priming seed germination; and enhancing photosynthesis. Future prospects are also presented.

 

THE GENERATION OF HYDROGEN SULFIDE

A number of studies have shown that many plant species can generate H2S, suggesting that it may be an endogenous chemical, suitable to act as a signaling molecule [1]. Wilson et al. [8] found, using a sulfur-specific flame photometric detector, that cucumber, squash, pumpkin, soybean, and cotton, amongst other plants, were able to generate H2S. Additionally, the rate of H2S emission was substantially increased when leaves were fed with sulfate through their petioles or when the plant roots were mechanically damaged [2]. Using cucumber as a model species, Sekiya et al. [9] also illustrated that young leaves emitted much more H2S than mature leaves. Furthermore, Rennenberg [2] found that pumpkin leaves emitted H2S if supplied with sulfate, sulfite, cysteine, or SO2, but different metabolic routes were used for different sulfur sources.

Further results illustrated that cysteine-synthesizing and degrading enzymes, such as O-acetyl-L-serine (thiol) lyase (OAS-TL; EC 4.2.99.8), L-cysteine desulfhydrase (L-CD; EC 4.4.1.1), and 3-mercaptopyruvate sulfurtransferase (MS; EC 2.8.1.2) are closely related to H2S production in plants [1]. L-CD specifically metabolizes L-cysteine to produce H2S, pyruvate, and ammonium [1]. L-CD activity and expression can be up-regulated when plants are attacked by pathogen, and this enzyme could be a key factor in releasing H2S during a plant defense response [1]. Additionally, in producing H2S, D-CD (EC 4.4.1.15) only decomposes D-cysteine, not L-cysteine (fig. 1).

 

THE PROPERTIES OF HYDROGEN SULFIDE

As mentioned above, H2S is a colorless and flammable gas. Its smell is characteristic of rotten eggs or the obnoxious odor of a blocked sewer. H2S is the sulfur analog of water molecule and can be oxidized in a series of reactions to form sulfur dioxide (SO2), sulfates, such as sulfuric acid, and elemental sulfur [1]. It has a molecular weight of 34.08 and a vapor density (d) of 1.19, i.e., it is heavier than air (d = 1.0). Its boiling point is 60.3°C, melting point is 82.3°C, and freezing point is 86°C [3]. 

Temperature also affects the solubility of H2S: at room temperature (20°C), one gram of H2S will dissolve in 242 mL of H2O, 94.3 mL of absolute ethanol, or 48.5 mL of diethyl ether. H2S is a highly lipophilic molecule, which easily penetrates lipid bilayer of cell membranes. H2S also evaporates relatively easy from aqueous solutions (vapor pressure = 18.75 × 105 Pa) [1]. It is a weak acid in aqueous solution with an acid dissociation constant (pKa) of 6.76 at 37°C. It can dissociate into H+ and hydrosulfide anion (HS), which in turn may dissociate into H+ and sulfide anion (S2) in the following reaction: H2S  H+ + HS  2 H+ + S2 [1].

 

HYSIOLOGICAL FUNCTIONS OF HYDROGEN SULFIDE

Mediator of stomatal movements

The loss of water from a plant occurs mainly through leaf stomata; stomatal movements involve many second messengers, such as Ca2+, H2O2, NO, ABA, and H2S cross-talking with each other; it is a key factor affecting transpiration in plants (fig. 2). Lisjak et al. [3] investigated the effects of NaSH and GYY4137 on stomatal closure in A. thaliana and found that NaSH and GYY4137 reduced the accumulation of NO in guard cells, which in turn caused stomatal opening in the light and prevented stomatal closure in the dark. Similarly, both NaSH and GYY4137 reduced the accumulation of NO induced by ABA treatment of leaf tissues in A. thaliana [10]. These results suggest a mode of action for H2S in plant cell signaling pathways. Additionally, the H2S scavenger hypotaurine and H2S synthesis inhibitors (aminooxyacetic acid (AOA), hydroxylamine, potassium pyruvate, and ammonia) inhibited drought-induced stomatal closure [1]. Moreover, drought stress enhanced the level of hydrogen peroxide (H2O2) in guard cells and increased the expression and activity of D-/L-CD as well as the content of H2S in leaves but had no significant effect in mutants atrbohD, atrbohF, and atrbohD/F [1]. In contrast, the H2O2 scavenger ascorbic acid and inhibitors of H2O2 synthesis (salicylhydroxamic acid (SHAM) and diphenylene iodonium (DPI)) decreased drought-induced H2S production and the activity of D-/L-CD in leaves [1]. In addition to these effects, Liu et al. [10] also found similar results in A. thaliana and Hou et al. [4] in V. faba using pharmacological treatments combined with laser scanning confocal microscopy (LSCM) and spectrophotography. These results implied that H2S may function downstream of H2O2 in the signal transduction pathway of stomatal closure in plants.

Interestingly, Ye et al. [11] found that NaHS caused stomatal closure in the light, and NaHS was able to induce H2O2 generation in guard cell cytoplasm and leaves of A. thaliana and the H2O2 scavenger ascorbic acid and H2O2 synthesis inhibitors SHAM and DPI all prevented H2S-induced stomatal closure and the level of H2O2 raised in guard cells and leaves. Additionally, the effects of NaHS were more significant in atrbohD, atrbohF, atpao2, and atpao4 mutants than in wild type, while in Arabidopsis overexpressing AtPAO2, AtPAO4 they were less pronounced [11]. These results showed that H2O2 produced by NADPH oxidase (NOX), cell wall peroxidase, and polyamine oxidase are involved in the signal transduction pathway of H2S-induced stomatal closure in A. thaliana. To study the interaction between ABA and H2S in stomatal movements, Liu et al. [10] reported that pretreatment with ABA increased L-/D-CD activity, which in turn induced H2S generation and stomatal closure in A. thaliana, while AOA, NH2OH, C3H3KO3+, and NH3 reduced the L-/D-CD activity increase and H2S generation induced by ABA. 

 

Mediating the adaptation to abiotic stresses

Plants are constantly exposed to various biotic and abiotic stresses due to sessile nature. Abiotic stresses, including heavy metals, salinity, drought, extreme temperatures, and mechanical stimulation, are major causes of crop failure worldwide [12]. Here, the adaptive mechanisms of plants to abiotic stresses involving H2S are presented (fig. 3) [13].

Heavy metal tolerance. Heavy metals (HM), such as Cd, Cr, Cu, Hg, and Pb, are conventionally defined as elements with metallic properties and an atomic number >20 [12]. Heavy metal toxicity is one of the major abiotic stresses leading to hazardous effects on plants. A common consequence of HM toxicity is the excessive ROS accumulation resulting in oxidative stress, that is, peroxidation of lipids, oxidation of proteins, inactivation of enzymes, DNA damage, and so forth [12]. Higher plants have evolved a sophisticated antioxidant defense system to scavenge ROS [14]. Aluminum (Al) is one of the major HM that limits plant growth. In barley seedlings, pretreatment with sodium hydrosulfide (NaHS) had significant rescue effects on Al-induced inhibition of root elongation, which was correlated well with the decrease in the Al accumulation in seedlings [15]. Additionally, NaHS pretreatment significantly alleviated Al-induced citrate secretion and oxidative stress as indicated by lipid peroxidation, as well as ROS burst through the activation of the antioxidant system [14]. In wheat, Zhang et al. [16] also obtained similar results. Alternatively, in wheat (Triticum aestivum), the application of exogenous NaHS could alleviate a decrease in the percentage of germination of wheat seeds under chromium (Cr) stress in a dose-dependent manner and enhance the activities of amylase and esterase, as well as antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and guaiacol peroxidase (POD), whereas reduced the Cr-induced increase in lipoxygenase activity and overproduction of MDA as well as H2O2, and sustained slightly the higher content of endogenous H2S [16]. In addition, NaHS alleviated the inhibitory effect of Cu in wheat in a dose-dependent manner. It was verified that H2S or HS rather than other sulfur-containing components derived from NaHS attribute to the potential role in promoting seed germination against Al stress [16]. Further experiments showed that NaHS could promote amylase and esterase activities, reduce Cu-induced disturbance of the plasma membrane integrity in the radicle tips, and sustain the lower levels of MDA and H2O2 in germinating seeds [16]. Additionally, NaHS pretreatment increased SOD and CAT activities and decreased that of lipoxygenase. These results consist with the response to Cr stress [16]. In addition, B toxicity in cucumber (Cucumis sativus) seedlings significantly inhibited root elongation and increased the activity of pectin methylesterase (PME) and up-regulated expression of genes encoding PME (CsPME) and expansin (CsExp), while these negative effects were substantially alleviated by treatment with H2S donor sodium hydrosulfide (NaHS) [17]. 

Salt tolerance. Common consequences of salt stresses lead to (1) osmotic stress, (2) ion toxicity, (3) nutrient imbalance, and (4) oxidative stress. Soil salinity is a major abiotic stress in plant agriculture worldwide. This has led to research of salt tolerance with the aim of improving crop plants. Pretreatment with NaHS and NO donor sodium nitroprusside (SNP) could significantly attenuate the inhibition of alfalfa (Medicago sativa) seed germination and thereafter seedling growth inhibition under 100 mM NaCl stress and an increase in the ratio of potassium (K) to sodium (Na) in the root parts [18]. In addition, isozymatic activities or corresponding transcripts of antioxidant enzymes, including SOD, CAT, POD, or APX, were activated differentially by NaHS, thus resulting in the alleviation of oxidative damage [17]. Further experiments found that the addition of the specific NO scavenger, 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt (cPTIO), reversed above protective roles, implying that H2S-induced protective effects might be related to the induction of endogenous NO [18].

Additionally, in salt-sensitive wheat cultivar LM15, Bao et al. [19] examined the effect of exogenous hydrogen sulfide on the seed germination rate, germination index, vigor index, and seedling growth under salt stress, and the results showed that seed pretreated with exogenous H2S could alleviate the NaCl-induced seed germination and seedling growth inhibition, as well as treatment with 0.01, 0.05, 0.09, and 0.13 mM NaHS for 12 h also significantly alleviated the inhibition of seed germination rate, germination index, vigor index, and growth of wheat seedlings under 100 mM NaCl stress in a concentration-dependent manner.

Drought tolerance. Drought stress, namely, water deficiency, is one of the most important environmental factors that limits plant growth, development, and production. Pretreatment with sodium hydrosulfide decreased the MDA content and electrolyte leakage induced by water deficiency in plants compared to control [20]. Meanwhile, the application of NaHS increased the activities of antioxidant enzymes, such as APX, glutathione reductase, dehydroascorbate reductase, and -glutamylcysteine synthetase, as well as the contents of reduced ascorbic acid, reduced glutathione, total ascorbate, and total glutathione under water stress compared to the control without NaHS treatment [20]. As mentioned above, L-CD and D-CD are identified as being mainly responsible for the degradation of cysteine in order to generate H2S. The expression regulation of corresponding genes and their relationship to drought tolerance in Arabidopsis were investigated, and the results showed that the expression pattern of L-/D-CD was similar to that of drought-associated genes induced by dehydration and fumigation with H2S stimulated further the expression of drought-associated genes [21]. In addition, drought stress also significantly induced an increased H2S production and this process was reversed by rewatering. Further experiments found that, after treatment with NaHS, seedlings showed a higher survival rate and displayed a substantial reduction in the size of the stomatal aperture compared to the control [21].

Using PEG 6000-mimicked osmotic stress, Zhang et al. [22] found that seed germination dropped gradually with the enhancement of osmotic stress, while NaHS treatment could stimulate wheat seed germination under osmotic stress in a dose-dependent manner. Na+ and various sulfur-containing components, such as S2–, SO42, SO32, HSO4–, and HSO3–, were not able to improve seed germination as NaHS did, confirming H2S or HS– derived from NaHS contributed to the protective roles [22]. Further experiments showed that NaHS treatment significantly increased CAT and APX activities, reduced lipoxygenase activity, and MDA and hydrogen peroxide accumulation in seeds. Meanwhile, the H2S donor treatment could retain the higher levels of endogenous H2S in wheat seeds under osmotic stress [22]. In addition to these, García-Mata and Lamattina [23] also found that, in V. faba (L.) var. major and Impatiens walleriana Hook. f., H2S treatment could increase relative water content (RWC) and protect plants against drought stress.

Heat tolerance. High temperature has already become a noticeable abiotic stress factor limiting crop yield. Many researchers concentrated their attention on heat tolerance of plants, especially crop plants. Christou et al. [24] tested whether hydroponic pretreatment of strawberry (Fragaria  ananassa cv. Camarosa) roots with 10 mM NaHS for 48 h could induce long-lasting priming effects and tolerance to subsequent exposure to heat stress at 42°C applied for 8 h. NaHS pretreatment of roots resulted in a significantly increased leaf chlorophyll fluorescence, stomatal conductance, and relative leaf water content, as well as in the reduced ion leakage and lipid peroxidation levels in comparison with plants directly subjected to heat stress. Our previous study it has been found that NaHS pretreatment significantly increased the survival percentage of tobacco suspension cultured cells under heat stress and regrowth ability after heat stress and alleviated a decrease in cell vitality, an increase in electrolyte leakage and MDA accumulation [7]. In addition, NaHS-induced heat tolerance was markedly strengthened by the application of exogenous Ca2+ and its ionophore A23187, while heat tolerance was weakened by the addition of the Ca2+ chelator EGTA, plasma membrane channel blocker La3+, as well as calmodulin (CaM) antagonists, chlorpromazine (CPZ) and trifluoperazine (TFP), but intracellular channel blocker ruthenium red (RR) did not [7]. In maize, we also found that pretreatment with NaHS markedly improved the germination percentage of seeds and the survival percentage of seedlings under heat stress and alleviated an increase in the electrolyte leakage from roots, a decrease in tissue vitality, and the accumulation of MDA in coleoptiles of maize seedlings [6]. In addition, pretreatment with NaHS could improve the activity of Δ1-pyrroline-5-carboxylate synthetase (P5CS) and reduce proline dehydrogenase (ProDH) activity, which in turn induced the accumulation of endogenous proline in maize seedlings [6]. Also, the application of proline could enhance endogenous proline content, followed by the increase in the survival percentage of maize seedlings under heat stress [6]. These results suggest that NaHS pretreatment could improve plant heat tolerance and the acquisition of this heat tolerance may be involved in calcium messenger system and proline accumulation. Interestingly, in animal systems, Miller and Roth [25] found that H2S treatment can increase thermotolerance and lifespan of Caenorhabditis elegans.

 

INVOLVING IN ORGANOGENESIS AND GROWTH

It is well known that organogenesis is regulated by a number of interacting factors, among which genotypic and plant hormonal factors are essential. In recent years, many researchers reported that H2S is involved in plant organogenesis and growth. Lin et al. [26] found that NaHS treatment could up-regulate target genes responsible for haem oxygenase-1/carbon monoxide (HO-1/CO)-induced adventitious root formation. In particular, CsDNAJ-1 and CsCDPK1/5 in cucumber bring about the induction of cucumber HO-1 transcripts (CsHO-1) and increase its protein level, which in turn promotes adventitious root formation. When cucumber explants were treated with HO-1 inducer haemin and NaHS in combination with the specific inhibitor of HO-1 zinc protoporphyrin IX, the above inducible effects were significantly suppressed [26]. However, hypotaurine, the H2S scavenger, could not influence the haemin- and CO-induced adventitious rooting in IAA-depleted cucumber explants [26]. Taken together, the above results suggest that HO-1 was involved in H2S -induced cucumber adventitious root formation. 

Alternatively, Li et al. [27] also reported that a low concentration of H2S (0~40 µM) could increase the P. sativum embryo root length, the content of root tip soluble protein, the activities of SOD, APX, and POD, as well as the survival rate of root border cells. In contrast, when the concentration of H2S was increased from 60 to 80 µM, the above indices all reduced. In addition to HM tolerance, Zhang et al. [28] found that pretreatment with NaHS could promote root organogenesis in Ipomoea batatas, Salix matsudana, and Glycine max. Moreover, Chen et al. [29] also found that Spinacia oleracea seedlings treated with various NaHS concentrations for 30 days exhibited a substantial increase in seedling growth. Thus, H2S might play an important role in the such physiological process in plants as organogenesis and growth.

 

REGULATION OF SENESCENCE

Plant senescence is a process when the physiological functions of cells, organs, or plant as a whole gradually weaken. Senescent cut flowers, in particular, has a short vase life, which limits efficient marketing of economically valuable ornamental plants [30]. The vase life of cut flowers is influenced by many internal factors, such as plant hormones and other endogenous regulators. Zhang et al. [30] investigated the effects of H2S on senescence of cut flowers and branches of Erigeron annuus (L.), Euonymus maackii Rupr., Hibiscus syriacus L., Liriope spicata (Thump.), Loropetalum chinense (R. Br.), Punica granatum L., Rosa chinensis Jacq., and Salix matsudana Koidz., and the results showed that cut explants of these plants cultured in the solution containing various concentrations of NaHS could delay flower opening and senescence in a dose-dependent manner. The level of MDA as an indicator of oxidative damage to cells was inversely related to endogenous H2S concentration in explants, while senesced flowers had the higher levels of MDA and the lower amounts of H2S. In addition, NaHS treatment increased the activities of CAT, SOD, APX, and POD and sustained much lower levels of H2O2 and O2• in cut flowers of E. annuus and explant leaves of S. matsudana [30]. These data imply that H2S treatment could improve longevity of cut flowers and this improvement involved in increase in activity of antioxidant enzymes in plants.

 

PRIMING AGENT OF SEED GERMINATION

A main agricultural goal is to obtain rapid and uniform germination and seedling emergence once seeds are sown. To increase the performance of commercial seed lots, the seed industry practices invigoration treatments referred to as seed priming, which have proved successful at invigorating the performance of low-vigor seeds [5]. As discussed above, pretreatment with H2S could promote seed germination and improve germination percentage of wheat seeds both under normal condition and under heavy metal, such as Cr, Al3+, and Cu2+, stress, as well as this promotive effects are related to strengthen the activities of amylase and antioxidant enzymes, such as SOD, CAT, APX, and POD [15, 16]. Our previous work also found that soaking in H2O2 greatly improved germination percentage of J. curcas seeds, stimulated the increase of L-CD activity, which in turn induced the accumulation of H2S [5]. In contrast, pretreatment with AOA, the inhibitor of H2S biosynthesis, eliminated the H2O2 stimulated increase of L-CD activity and the accumulation of H2S, as well as improved germination percentage [5]. In addition, exogenously applied H2S also could improve germination percentage of J. curcas [5]. These results suggested that H2S might act as a priming agent to promote seed germination and improve germination percentage both under normal conditions and under abiotic stress.

 

ENHANCEMENT OF PHOTOSYNTHESIS

As mentioned above, H2S could promote stomatal opening in various plant species, which in turn indirectly enhances photosynthesis [1]. Chen et al. [29] investigated the role of H2S in modulating photosynthesis of S. oleracea seedlings, and the results showed that NaHS treatment could increase the chlorophyll content in leaves, photosynthesis in a dose-dependent manner, the number of granal lamellae stacking into the functional chloroplast, the light saturation point, the maximum net photosynthetic rate, and carboxylation efficiency, as well as the maximal photochemical efficiency of photosystem II (Fv/Fm) reached their maximal values, whereas the light compensation point and dark respiration decreased significantly under the optimal NaHS concentration. In addition, the activity of ribulose-1,5-bisphosphate carboxylase (Rubisco) and the protein expression of the Rubisco large subunit were also significantly enhanced by NaHS [29]. Further experiments using quantitative real-time PCR showed that the genes encoding the Rubisco large subunit (RBCL), small subunit (RBCS), ferredoxin thioredoxin reductase, ferredoxin, thioredoxin m, thioredoxin f, NADP-malate dehydrogenase, and O-acetylserine(thiol)lyase were up-regulated, but genes encoding serine acetyltransferase, glycolate oxidase, and cytochrome oxidase were down-regulated after exposure to the optimal concentration of H2S [29]. These data suggest that increases in Rubisco activity and the function of thiol redox modification may underlie the amelioration of photosynthesis and that H2S plays an important role in plant photosynthesis regulation by modulating the expression of genes involved in photosynthesis and thiol redox modification.

 

CONCLUSIONS AND PERSPECTIVES

H2S fulfills multiple functions, modulating physiological processes in plants. It operates as a mediator of stomatal movements; affects tolerance to heavy metals, salt, drought, and heat stresses; is involved in plant organogenesis and growth; regulates senescence; is a priming agent of seed germination; and enhances photosynthesis. However, despite the critical role of H2S throughout the plant life cycle and in responses against adverse environmental cues, many questions remain to be answered. What are the physiological concentrations of H2S? Which environmental stimuli trigger H2S accumulation? How the cell perceives H2S? The use of transgenic plants that are impaired in H2S generation, such as lcd mutants, will be invaluable in illustrating further the physiological role of H2S. Additionally, the post-genomic developments, transcriptomics and proteomics, will facilitate further insights into cellular responses to H2S; and novel signaling role of H2S and its interaction with other signals like Ca2+, H2O2, NO, and phytohormones will be no doubt revealed in future study.

The work of some researchers might not have been described in this article due to the limited space. 

This research was supported by the Natural Science Foundation of Yunnan Province of China (2010ZC066).

 REFERENCES

1. Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed // Physiol. Rev. 2012. V. 92. P. 791–896.

2. Rennenberg H. The fate excess of sulfur in higher plants // Annu. Rev. Plant Physiol. 1984. V. 35. P. 121–153.

3. Lisjak M., Srivastava N., Teklic T., Civale L., Lewandowski K., Wilson I., Wood M.E., Whiteman M., Hancock J.T. A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation // Plant Physiol. Biochem. 2010. V. 48. P. 931–935.

4. Hou Z.H., Liu J., Hou L.X., Li X.D., Liu X. H2S may function downstream of H2O2 in jasmonic acid-induced stomatal closure in Vicia faba // Chinese Bull. Bot. 2011. V. 46. P. 396–406.

5. Li Z.G., Gong M., Liu P. Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas // Acta Physiol. Plant. 2012. V. 34. P. 2207–2213.

6. Li Z.G., Ding X.J., Du P.F. Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline // J. Plant Physiol. 2013. doi 10.1016/j.jplph.2012.12.018

7. Li Z.G., Gong M., Xie H., Yang L., Li J. Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin // Plant Sci. 2012. V. 185/186. P. 185–189.

8. Wilson L.G., Bressan R.A., Filner P. Light-dependent emission of hydrogen sulphide from plants // Plant Physiol. 1978. V. 61. P. 184–189.

9. Sekiya J., Schmidt A.,Wilson L.G., Filner P. Emission of hydrogen sulfide by leaf tissue in response to L-cysteine // Plant Physiol. 1982. V. 70. P. 430–436.

10. Liu J., Hou L.X., Liu G.H., Liu X., Wang X.C. Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana // Chinese Sci. Bull. 2011. V. 56. P. 3547–3553.

11. Ye Q., Hou Z.H., Jing L., Liu R.Q., Liu X. H2O2 involvement in H2S-induced stomatal closure of Arabidopsis thaliana L. // Chinese Plant Physiol. J. 2011. V. 47. P. 1195–1200.

12. Yadav S.K. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants // S. Afr. J. Bot. 2010. V. 76. P. 167–179.

13. Hancock J.T., Lisjak M., Teklic T., Wilson I.D., Whiteman M. Hydrogen sulphide and signalling in plants // CAB Rev. Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 2011. V. 6. P. 1–7.

14. Li Z.G., Gong M. Mechanical stimulation-induced cross-adaptation in plants: an overview // J. Plant Biol. 2011. V. 54. P. 358–364.

15. Chen J., Wang W.H., Wu F.H., You C.Y., Liu T.W., Dong X.J., He J.X., Zheng H.L. Hydrogen sulfide alleviates aluminum toxicity in barley seedlings // Plant Soil. 2012. doi 10.1007/s11104-012-1275-7

16. Zhang H., Tan Z.Q., Hu L.Y., Wang S.H., Luo J.P., Jones R.L. Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings // J. Integr. Plant Biol. 2010. V. 52. P. 556–567.

17. Wang B.L., Shi L., Li Y.X., Zhang W.H. Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings // Planta. 2010. V. 231. P. 1301–1309.

18. Wang Y.Q., Li L., Cui W.T., Xu S., Shen W.B., Wang R. Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway // Plant Soil. 2012. V. 351. P. 107–119.

19. Bao J., Ding T.L., Jia W.J., Wang L.Y., Wang B.S. Effect of exogenous hydrogen sulfide on wheat seed germination under salt stress // Modern Agric. Sci. Technol. 2011. V. 20. P. 40–42.

20. Shan C.J., Zhan, S.L., Li D.F., Zhao Y.Z., Tian X.L., Zhao X.L., Wu Y.X., Wei X.Y., Liu R.Q. Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress // Acta Physiol. Plant. 2011. V. 33. P. 2533–2540.

21. Jin Z.P., Shen J.J., Qiao Z.J., Yang G.D., Wang R., Pei Y.X. Hydrogen sulfide improves drought resistance in Arabidopsis thaliana // Biochem. Biophys. Res. Commun. 2011. V. 414. P. 481–486.

22. Чжан Ш., Ван М.И., Ху Л.Я., Ван С.Ш., Ху К.Д., Бао Л.И., Ло И.П. Сероводород стимулирует прорастание семян пшеницы при осмотическом стрессе // Физиология растений. 2010. Т. 57. С. 571–579.

23. García-Mata C., Lamattina L. Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling // New Phytol. 2010. V. 188. P. 977–984.

24. Christou A., Manganaris G., Papadopoulos I., Fotopoulos V. The importance of hydrogen sulfide as a systemic priming agent in strawberry plants grown under key abiotic stress factors // Abst. 4th Int. Conf. “Plant Abiotic Stress: From Systems Biology to Sustainable Agriculture” (November 17–19, 2011). Limassol, Cypris, 2011. P. 47.

25. Miller D.L., Roth M.B. Hydrogen sulfide increases thermotolerance and lifespan in Caenorhabditis elegans // Proc. Natl. Acad. Sci. USA. 2007. V. 104. P. 20 618–20 622.

26. Lin Y.T., Li M.Y., Cui W.T., Lu W., Shen W.B. Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation // J. Plant Growth Regul. 2012. doi 10.1007/s00344-012-9262-z

27. Li D.B., Xiao Z.X., Liu L.X., Wang J.C., Song G.L., Bi Y.R. Effects of exogenous hydrogen sulfide (H2S) on the root tip and root border cells of Pisum sativum // Chinese Bull. Bot. 2010. V. 45. P. 354–362.

28. Zhang H., Tang J., Liu X.P., Wang Y., Yu W., Peng W.Y., Fang F., Ma D.F., Wei Z.J., Hu L.Y. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max // J. Integr. Plant Biol. 2009. V. 51. P. 1084–1092.

29. Chen J., Wu F.H., Wang W.H., Zheng C.J., Lin G.H., Dong X.J., He J.X., Pei Z.M., Zheng H.L. Hydrogen sulfide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings // J. Exp. Bot. 2011. V. 62. P. 4481–4493.

30. Zhang H., Hu S.L., Zhang Z.J., Hua L.Y., Jiang C.X., Wei Z.J., Liu J., Wang H.L., Jiang S.T. Hydrogen sulfide acts as a regulator of flower senescence in plants // Postharvest Biol. Technol. 2011. V. 60. P. 251–257.

 FIGURE CAPTIONS

 

Fig. 1. Hydrogen sulfide biosynthesis in plants.

L-cysteine desulfhydrase (L-CD; EC 4.4.1.1) or D-cysteine desulfhydrase (D-CD; EC 4.4.1.15) specifically metabolizes L-cysteine or D-cysteine to produce H2S, pyruvate, and ammonium or sulfite is reduced by sulfite reductase (SiR; EC 1.8.7.1) to H2S in plants (adapted from Wang [1]). 

 

Fig. 2. Schematic diagram of H2S-regulated stomatal movements in plants.

H2S controls stomatal movements via crosstalk with second messengers, such as ABA, Eth, NO, H2O2, Ca2+. Arrows () indicate positive effects, blunt line (├) indicates negative effect, question mark (?) indicates the interaction between H2S and Ca2+ is not confirmed. ABA  abscisic acid; Eth  ethylene; L-/D-CD  L-/D-cysteine desulfhydrase; NOX  NADPH oxidase. 

 

Fig. 3. Part mechanism of H2S-induced abiotic stress in plants.

H2S can be present in the environment, be generated by plant cells, be removed by plant cells, and there are many effects and responses. Up and down arrows indicate positive and negative effects, respectively. APR  adenosine-5-phosphosulfate reductase; L-/D-CD  L-/D-cysteine desulfhydrase; NO  nitric oxide; SiR  sulfite reductase (adapted from Hancock et al. [13]).