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Hydrogen sulfide: a versatile regulator of environmental stress in plants

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Abstract

In mammalian cells, hydrogen sulfide (H2S) has been identified as the third gasotransmitter after nitric oxide and carbon monoxide. Overwhelming evidence has proven that H2S also participates in diverse physiological and biochemical processes within the organism and exert specific functions in plants. A number of reports illustrated that H2S could improve plants ability of adapting to the multiple environmental stimuli by alleviating injuries and toxicities caused by the stressful conditions. It also participated in specific physiological, developmental and metabolic processes, such as the regulation of stomatal movement and drought tolerance, senescence and maturation, and lateral root formation. In this article, latest research progresses in biosynthetic and metabolic pathways of H2S in plants as well as corresponding physiological functions were summarized. We also discussed the potential molecular mechanism of interaction between H2S and other signaling molecules as well as the H2S-modifying protein activities. Finally, we prospected possible future work for H2S in plants.

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Abbreviations

ABA:

Abscisic acid

Al:

Aluminum

AOA:

Aminooxyacetic acid

APX:

Ascorbate peroxidase

AsA:

Ascorbate

AtNFS1/AtNifS:

Arabidopsis thaliana nitrogen fixation S

AtNFS2/AtSUF:

Arabidopsis chloroplastic nitrogen fixation S

CaM:

Calmodulin

cAMP:

Cyclic adenosine monophosphate

CAT:

Cysteine aminotransferase

CBS:

Cystathionine-β-synthase

CBSX:

Cystathionine-β-synthase domain-containing protein

CDes:

Cysteine desulfhydrases

cPTIO:

2-(4-Carboxyphenyl)-4,4,5,5-tetramethylimidazoline-l-oxyl-3-oxide

CSE:

Cystathionine-γ-lyase

DAF-FM-DA:

4,5-Diaminoflorescein diacetate

DHAR:

Dehydroascorbate reductase

DTT:

Dithiothreitol

EDTA:

Ethylene diamine tetraacetic acid

FTS:

Ferredoxin-Trx system

G6PDH:

Glucose-6-phosphate dehydrogenase

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

GSH:

Glutathione

GSNO:

S-Nitrosoglutathione

GR:

Glutathione reductase

GYY4137:

Morpholin-4-ium 4 phosphinodithioate

H2S:

Hydrogen sulfide

H2O2 :

Hydrogen peroxide

HT:

Hypotaurine

IAA:

Indole acetic acid

l-DES:

l-Cystine desulfydrase

MDA:

Malondialdehyde

3-MST:

3-Mercapto pyruvate sulfurtransferase

MDHAR:

Monodehydroascorbate reducatase

NaHS:

Sodium hydrosulfide

NR:

Nitrate reductase

nia1/2:

Nitrate reductase 1/2

NO:

Nitric oxide

NTS:

NADP-Trx system

OASTL:

O-Acetylserine(thiol)lyase

O2 :

Superoxide anion

POD:

Peroxidase

PME:

Pectin micronutrient

ProDH:

Proline dehydrogenase

P5CS:

1-Pyrroline-5-carboxylate synthetase

ROS:

Reactive oxygen species

SAVs:

Senescence-associated vacuoles

SAT:

Serine acetyltransferase

SKOR:

Shaker-like K+ outward-rectifying K channels

SNAP:

S-Nitroso-N-acetylpenicillamine

SNP:

Sodium nitroprusside

SOD:

Superoxide dismutase

References

  • Aida K, Tokuyama T, Uemura T (1969) The role of cysteine desulphhydrase and cysteine synthase in the evolution of hydrogen sulphide in pantothenic acid deficient yeast. Antonie Van Leeuwenhoek 35(Suppl 1):15–16

    Google Scholar 

  • Álvarez C, Bermúdez MÁ, Romero LC, Gotor C, García I (2012a) Cysteine homeostasis plays an essential role in plant immunity. New Phytol 193:165–177

    Article  PubMed  CAS  Google Scholar 

  • Álvarez C, Calo L, Romero LC, García I, Gotor C (2010) An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Álvarez C, García I, Moreno I, Pérez-Pérez ME, Crespo JL, Romero LC, Gotor C (2012b) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Aroca A, Serna A, Gotor C, Romero LC (2015) S-Sulfhydration: a cystein posttranslational modification in plant systems. Plant Physiol 168:334–342

    Article  CAS  PubMed  Google Scholar 

  • Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-Nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    Article  CAS  PubMed  Google Scholar 

  • Barroso C, Vega JM, Gotor C (1995) A new member of the cytosolic O-acetylserine(thiol)lyase gene family in Arabidopsis thaliana. FEBS Lett 365:1–5

    Article  Google Scholar 

  • Baskar R, Bian J (2011) Hydrogen sulfide gas has cell growth regulatory role. Eur J Pharmacol 656:5–9

    Article  CAS  PubMed  Google Scholar 

  • Beja-Tal S, Borochov A (1994) Age-related changes in biochemical and physical properties of carnation petal plasma membranes. J Plant Physiol 143:195–199

    Article  CAS  Google Scholar 

  • Bonner ER, Cahoon RE, Knapke SM, Jez JM (2005) Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 280:38803–38813

    Article  CAS  PubMed  Google Scholar 

  • Borochov A, Cho MH, Boss WF (1994) Plasma membrane lipid metabolism of petunia petals during senescence. Physiol Plant 90:279–284

    Article  CAS  Google Scholar 

  • Borochov A, Woodson WR (1989) Physiology and biochemistry of flower petal senescence. Hortic Rev 11:15–43

    CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Burandt P, Schmidt A, Papenbrock J (2002) Three O-acetyl-l-serine(thiol)lyase isoenzymes from Arabidopsis catalyse cysteine synthesis and cysteine desulfuration at different pH values. J Plant Physiol 159:111–119

    Article  CAS  Google Scholar 

  • Calderwood A, Kopriva S (2014) Hydrogen sulfide in plants: from dissipation of excess sulfur to signaling molecule. Nitric Oxide 41:72–78

    Article  CAS  PubMed  Google Scholar 

  • Chaerle L, Saibo N, Van Der Straeten D (2005) Tuning the pores: towards engineering plants for improved water use efficiency. Trends Biotechnol 23:308–315

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Wang WH, Wu FH, You CY, Liu TW, Dong XJ, He JX, Zheng HL (2013) Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362:301–318

    Article  CAS  Google Scholar 

  • Cooper CE, Brown GC (2008) The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance. J Bioenerg Biomembr 40:533–539

    Article  CAS  PubMed  Google Scholar 

  • Dawood M, Cao F, Jiahanqir MM, Zhang G, Wu F (2012) Alleviation of aluminum toxicity by hydrogen sulfide is related to elevated ATPase, and suppressed aluminum uptake and oxidative stress in barley. J Hazard Mater 209–210:121–128

    Article  PubMed  CAS  Google Scholar 

  • Dorman DC, Moulin FJ-M, McManus BE, Mahle KC, Jmmes RA, Struve MF (2001) Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium. Toxicol Sci 65:18–25

    Article  Google Scholar 

  • Fang HH, Pei YX, Tian BH, Zhang LP, Qiao ZJ, Liu ZQ (2014) Ca2+ participates in H2S induced Cr6+ tolerance in Setaria italica. Chin J Cell Biol 36:758–765

    CAS  Google Scholar 

  • Ferreira-Silva SL, Voigt EL, Silva EN, Maia JM, Aragão TC, Silveira JAG (2012) Partial oxidative protection by enzymatic and non-enzymatic components in cashew leaves under high salinity. Biol Plant 56:172–176

    Article  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2010) Hydrogen sulfide, a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977–984

    Article  PubMed  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2013) Gssotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci 201(202):66–73

    Article  PubMed  CAS  Google Scholar 

  • Gupta KJ (2011) Protein S-nitrosylation in plants: photorespiratory metabolism and NO signaling. Sci Signal 4(154):jc1. doi:10.1126/scisignal.2001404

    CAS  PubMed  Google Scholar 

  • Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem 78:37–42

    Article  CAS  PubMed  Google Scholar 

  • Hanumappa M, Nguyen HT (2010) Genetic approaches toward improving heat tolerance in plants. In: Jenks MA, Wood AJ (eds) Genes for plant abiotic stress. Blackwell Publishing, Oxford, UK, pp 221–260

    Google Scholar 

  • Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65:151–155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hell R, Bork C, Bogdanova N, Frolov I, Hauschild R (1994) Isolation and characterization of two cDNAs encoding for compartment specific isoforms of O-acetylserine (thiol) lyase from Arabidopsis thaliana. FEBS Lett 351:257–262

    Article  CAS  PubMed  Google Scholar 

  • Helmy N, Prip-Buus C, Vons C, Lenoir V, Abou-Hamdan A, Guedouari-Bounihi H, Lombès A, Bouillaud F (2014) Oxidation of hydrogen sulfide by human liver mitochondria. Nitric Oxide 41:105–112

    Article  CAS  PubMed  Google Scholar 

  • Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166

    Article  CAS  PubMed  Google Scholar 

  • Hess DT, Stamler JS (2012) Regulation by S-nitrosylation of protein posttranslational modification. J Biol Chem 287:4411–4418

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hesse H, Lipke J, Altmann T, Höfgen R (1999) Molecular cloning and expression analyses of mitochondrial and plastidic isoforms of cysteine synthase (O-acetylserine(thiol)lyase) from Arabidopsis thaliana. Amino Acids 16:113–131

    Article  CAS  PubMed  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  CAS  PubMed  Google Scholar 

  • Hou Z, Liu J, Hou L, Li X, Liu X (2011) H2S may function downstream of H2O2 in jasmonic acid-induced stomatal closure in Vicia faba. Chin Bull Bot 46:396–406

    Article  CAS  Google Scholar 

  • Hu JL, Huang XH, Chen LC, Sun XW, Lu CM, Zhang LX, Wang YC, Zuo JR (2015) Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis. Plant Physiol 167:1734–1746

    Google Scholar 

  • Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 3:193–197

    Article  CAS  PubMed  Google Scholar 

  • Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486

    Article  CAS  PubMed  Google Scholar 

  • Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei YX (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    Article  CAS  PubMed  Google Scholar 

  • Jost R, Berkowitz O, Wirtz M, Hopkins L, Hawkesford MJ, Hell R (2000) Genomic and functional characterization of the oas gene family encoding O-acetylserine (thiol) lyases, enzymes catalyzing the final step in cysteine biosynthesis in Arabidopsis thaliana. Gene 253:237–247

    Article  CAS  PubMed  Google Scholar 

  • Kabil O, Motl N, Banerjee R (2014) H2S and its role in redox signaling. Biochim Biophys Acta 1844:1355–1366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kida K, Yamada M, Tokuda K, Marutani E, Kakinohana M, Kaneki M, Ichinose F (2011) Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson’s disease. Antioxid Redox Signal 15:343–352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kimura H (2000) Hydrogen sulfide induces cyclic AMP and modulates the NMDA recrptor. Biochem Biophys Res Commun 267:129–133

    Article  CAS  PubMed  Google Scholar 

  • Kimura H (2014) The physiological role of hydrogen sulfide and beyond. Nitric Oxide 41:4–10

    Article  CAS  PubMed  Google Scholar 

  • Kimura Y, Kimura H (2004) Hydrogen sulfide protects neurons from oxidative stress. FASEB J 18:1165–1167

    CAS  PubMed  Google Scholar 

  • Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324

    Article  CAS  PubMed  Google Scholar 

  • Kolluru GK, Shen X, Bir SC, Kevil CG (2013) Hydrogen sulfide chemical biology: pathophysiological roles and detection. Nitric Oxide 35:5–20

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kubo S, Kurokawa Y, Doe I, Masuko T, Sekiguchi F, Kawabata A (2007) Hydrogen sulfide inhibits activity of three isoforms of recombinant nitric oxide synthase. Toxicology 241:92–97

    Article  CAS  PubMed  Google Scholar 

  • Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Van Montagu M (2001) A Mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lai DW, Mao Y, Zhou H, Li F, Wu M, Zhang J, He Z, Cui W, Xie Y (2014) Endogenous hydrogen sulfide enhances salt tolerance by coupling the reestablishment of redox homeostasis and preventing salt-induced K+ loss in seedlings of Medicago sativa. Plant Sci 225:117–129

    Article  CAS  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:628–695

    Google Scholar 

  • Leon S, Tournaine B, Briat JF, Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366:557–564

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li ZG, Ding XJ, Du PF (2013a) Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2011) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185–186:185–189

    PubMed  Google Scholar 

  • Li J, Jia H, Wang J, Cao Q, Wen Z (2014) Hydrogen sulfide is involved in maintaining ion homeostasis via regulating plasma membrane Na+/H+ antiporter system in the hydrogen peroxide-dependent manner in salt-stress Arabidopsis thaliana root. Protoplasma 251:899–912

    Article  CAS  PubMed  Google Scholar 

  • Li L, Wang YQ, Shen WB (2012) Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. Biometals 25:617–631

    Article  CAS  PubMed  Google Scholar 

  • Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK (2008) Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117:2351–2360

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yang SZ, Long WB, Yang GX, Shen ZZ (2013b) Hydrogen sulphide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ 36:1564–1572

    Article  CAS  PubMed  Google Scholar 

  • Lin YT, Li MY, Cui WT, Lu W, Shen WB (2012) Haem oxygenase-1 is involved in hydrogen sulfide-induced cucumber adventitious root formation. J Plant Growth Regul 31:519–528

    Article  CAS  Google Scholar 

  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T, Civale L, Lewandowski K, Wilson I, Wood ME, Whiteman M, Hancock JT (2010) A novel hydrogen sulfide donor causes stomatal opening and reduces nitric oxide accumulation. Plant Physiol Biochem 48:931–935

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulphide: environmental factor or signaling molecule? Plant Cell Environ 36:1607–1616

    Article  CAS  PubMed  Google Scholar 

  • Lisjak M, Teklic T, Wilson ID, Wood ME, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 6:1444–1446

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mancardi D, Penna C, Merlino A, Del Soldato P, Wink DA, Pagliaro P (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide. Biochim Biophys Acta 1787:864–872

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang GD, Wang R, Snyder SH (2009) H2S Signals through protein S-sulfhydration. Sci Signal 2:72

    Google Scholar 

  • Nagasawa T, Ishii T, Kumagai H, Yamada H (1985) d-Cysteine desulfhydrase of Escherichia coli. Purification and characterization. Eur J Biochem 153:541–551

    Article  CAS  PubMed  Google Scholar 

  • Nagasawa T, Ishii T, Yamada H (1988) Physiological comparison of d-cysteine desulfhydrase of Escherichia coli with 3-chloro-d-alanine dehydrochlorinase of Pseudomonas putida CR 1–1. Arch Microbiol 149:413–416

    Article  CAS  PubMed  Google Scholar 

  • Olas B (2015) Hydrogen sulfide in signaling pathways. Clin Chim Acta 439:212–218

    Article  CAS  PubMed  Google Scholar 

  • Paliyath G, Droillard MJ (1992) The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol Biochem 30:789–812

    CAS  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants: from the field to the test tube and back. Plant Biol 9:582–588

    Article  CAS  PubMed  Google Scholar 

  • Pilon-Smits EA, Garifullina GF, Abdel-Ghany S, Kato S, Mihara H, Hale KL, Burkhead JL, Esaki N, Kurihara T, Pilon M (2002) Characterization of a NifS-like chloroplast protein from Arabidopsis. Implications for its role in sulfur and selenium metabolism. Plant Physiol 130:1309–1318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Polhemus DJ, Lefer DJ (2014) Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease. Circ Res 114:730–737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rennenberg H (1983) Cysteine desulfhydrase activity in cucurbit plants: simulation by preincubation with l- and d-cysteine. Phytochemistry 22:1557–1560

    Article  CAS  Google Scholar 

  • Rennenberg H, Arabatzis N, Grundel I (1987) Cysteine desulphydrase activity in higher plants: evidence for the action of l- and d-cysteine specific enzymes. Phytochemistry 26:1583–1589

    Article  CAS  Google Scholar 

  • Rennenberg H, Filner P (1983) Developmental changes in the potential for H2S emission in cucurbit plants. Plant Physiol 71:269–275

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Riemenschneider A, Weqele R, Schmidt A, Papenbrock J (2005) Isolation and characterization of a d-cysteine desulfhydrase protein from Arabidopsis thaliana. FEBS J 272:1291–1304

    Article  CAS  PubMed  Google Scholar 

  • Romero LC, Aroca MA, Serna A, Gotor C (2013a) Proteomic analysis of endogenous S-sulfhydration in Arabidopsis thaliana. Nitric Oxide 31:S23

    Article  Google Scholar 

  • Romero LC, Garcia I, Gotor C (2013b) l-Cysteine desulfhydrase1 modulates the generation of the signaling molecule sulfide in plant cytosol. Plant Signal Behav 8:e24007

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rubinstein B (2000) Regulation of cell death in flower petals. Plant Mol Biol 44:303–318

    Article  CAS  PubMed  Google Scholar 

  • Schmidt A (1982) A cysteine desulfhydrase from spinach leaves specific for d-cysteine. Zeitschrift fr Pflanzenphysiologie 107:301–312

    Article  CAS  Google Scholar 

  • Schmidt A, Erdle I (1983) A cysteine desulfhydrase specific for d-cysteine from the green alga Chlorella fusca. Zeitschrift für Naturforschung C 38:428–435

    Google Scholar 

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  PubMed  Google Scholar 

  • Scuffi D, Núñez A, Laspina N, Gotor C, Lamattina L, Garcia-Mata C (2014) Hydrogen sulfide generated by l-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sen N, Paul BD, Gadalla MM, Mustafa AK, Sen T, Xu R, Kin S, Snyder SH (2012) Hydrogen sulfide-linked Sulfhydration of NF-κB mediates its antiapoptotic actions. Mol Cell 45(1):13–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shan C, Liu H, Zhao L, Wang X (2014) Effects of exogenous hydrogen sulfide on the redox states of ascorbate and glutathione in maize leaves under salt stress. Biol Plant 58:169–173

    Article  CAS  Google Scholar 

  • Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protects cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550

    Article  CAS  PubMed  Google Scholar 

  • Shi HT, Ye TT, Chan ZL (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 74:99–107

    Article  CAS  PubMed  Google Scholar 

  • Shibuya N, Tanaka M, Yoshida M, Ogasawara Y, Togawa T, Ishii K (2009) 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid Redox Signal 11:703–714

    Article  CAS  PubMed  Google Scholar 

  • Singh VP, Singh S, Kumar J, Prasad SM (2015) Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate–glutathione cycle: possible involvement of nitric oxide. J Plant Physiol 181:20–29

    Article  CAS  PubMed  Google Scholar 

  • Stamler JS, Lamas S, Fang FC (2001) Nitrosylation, the prototypic redox-based signaling mechanism. Cell 106:675–683

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Wang R, Zhang X, Yu Y, Zhao R, Li Z, Chen S (2013) Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells. Plant Physiol Biochem 65:67–74

    Article  CAS  PubMed  Google Scholar 

  • Wahid A, Gelani S, Ashrf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wang R (2002) Two’s compay, three’s a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 16:1792–1798

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang BL, Shi L, Li YX, Zhang WH (2010) Boron toxicity is alleviated by hydrogen sulfide in cucumber (Cucumis sativus L.) seedlings. Planta 231:1301–1309

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Yun BW, Kwon E, Hong JK, Yoon J, Loake GJ (2006) S-Nitrosylation: an emerging redox-based post-translational modification in plants. J Exp Bot 57:1777–1784

    Article  CAS  PubMed  Google Scholar 

  • Wirtz M, Droux M, Hell R (2004) O-Acetylserine(thiol)lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55:1785–1798

    Article  CAS  PubMed  Google Scholar 

  • Xie YJ, Lai DW, Mao Y, Zhang W, Shen WB, Guan RZ (2013a) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54:737–746

    Article  CAS  PubMed  Google Scholar 

  • Xie YJ, Zhang C, Lai DW, Sun Y, Samma MK, Zhang J, Shen WB (2013b) Hydrogen sulfide delays GA-triggered programmed cell death in wheat aleurone layers by the modulation of glutathione homeostasis and heme oxygenase-1 expression. J Plant Physiol 171:53–62

    Article  PubMed  CAS  Google Scholar 

  • Xu S, Liu Z, Liu P (2014) Targeting hydrogen sulfide as a promising therapeutic strategy for atherosclerosis. Int J Cardiol 172:313–317

    Article  PubMed  Google Scholar 

  • Yang G, Zhao K, Ju Y, Mani S, Cao Q, Puukila S, Khaper N, Wu L, Wang R (2013) Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid Redox Signal 18:1906–1919

    Article  CAS  PubMed  Google Scholar 

  • Yoo KS, Ok SH, Jeong BC, Jung KW, Cui MH, Hyoung S, Lee MR, Song HK, Shin JS (2011) Single cystathionine β-synthase domain-containing proteins modulate development by regulating the thioredoxin system in Arabidopsis. Plant Cell 23:3577–3594

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156

    Article  CAS  Google Scholar 

  • Zhang H, Hu LY, Hu KD, He YD, Wang SH, Luo JP (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu SL, Zhang ZJ, Hu LY, Jiang CX, Wei ZJ, Liu J, Wang HL, Jiang ST (2011) Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharvest Biol Technol 60:251–257

    Article  CAS  Google Scholar 

  • Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Wang MJ, Hu LY, Wang SH, Hu KD, Bao LJ, Luo JP (2010) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57:532–539

    Article  CAS  Google Scholar 

  • Zhao WM, Zhang J, Lu YJ, Wang R (2001) The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener. EMBO J 20:6008–6016

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (31200195), the Fundamental Research Funds for the Central Universities (KYZ201529), Natural Science Foundation of Jiangsu Province (BK2012364), Specialized Research Fund for the Doctoral Program of Higher Education (20120097120019), Youth Sci-Tech Innovation Fund, Nanjing Agricultural University (KJ2012022), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Correspondence to Yanjie Xie.

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Communicated by P. Wojtaszek.

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Guo, H., Xiao, T., Zhou, H. et al. Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38, 16 (2016). https://doi.org/10.1007/s11738-015-2038-x

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  • DOI: https://doi.org/10.1007/s11738-015-2038-x

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