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Hydrogen Sulfide and Posttranslational Modification of Proteins: A Defense Strategy Against Abiotic Stress

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Hydrogen Sulfide and Plant Acclimation to Abiotic Stresses

Part of the book series: Plant in Challenging Environments ((PCE,volume 1))

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Abstract

Hydrogen sulfide (H2S), as a signaling gasotransmitter, has been reported to be involved in the regulation of diverse biological processes. Nevertheless, the underlying H2S-regulated mechanisms in plant biological functions are poorly understood. A new way of post-translational modification of proteins, named persulfidation, was found and used to explain the core mechanism of H2S action. Persulfidation results in the modification of cysteine residues on target proteins, via conversion of the thiol group into a persulfide group. Persulfidated proteins exhibit functional changes in enzyme activities and therefore, modified cysteine can interact with several other proteins and expresses greater reactivity due to the increased nucleophilicity of persulfide compared with the thiol group. Persulfidation is believed to play crucial role in the protective mechanisms through affecting antioxidant system, autophagy, and stomatal closure. In the present chapter the importance of persulfidation in H2S-mediated plant adaptive responses to various abiotic stresses and methods for the detection of protein persulfidation are presented. Also, the crosstalk of H2S, NO, and ROS has been analyzed, especially in relation to posttranslational modification of proteins.

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References

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alvarez C, García I, Moreno I et al (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amooaghaie R, Zangene-madar F, Enteshari S (2017) Role of two-sided crosstalk between NO and H2S on improvement of mineral homeostasis and antioxidative defense in Sesamum indicum under lead stress. Ecotox Environ Saf 139:210–218

    Article  CAS  Google Scholar 

  • Aroca A, Serna A, Gotor C et al (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Benito JM, Gotor C et al (2017a) Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. J Exp Bot 68:4915–4927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aroca A, Schneider M, Scheibe R et al (2017b) Hydrogen sulfide regulates the cytosolic/nuclear partitioning of glyceraldehyde-3-phosphate dehydrogenase by enhancing its nuclear localization. Plant Cell Physiol 58:983–992

    Article  CAS  PubMed  Google Scholar 

  • Aroca A, Gotor C, Romero LC (2018) Hydrogen sulfide signaling in plants: emerging roles of protein persulfidation. Front Plant Sci 9:1369

    Article  PubMed  PubMed Central  Google Scholar 

  • Astier J, Kulik A, Koen E et al (2012) Protein Snitrosylation: what’s going on in plants? Free Radic Biol Med 53:1101–1110

    Article  CAS  PubMed  Google Scholar 

  • Aubert S, Gout E, Bligny R et al (1996) Ultrastructural and biochemical characterization of autophagy in higher plant cells subjected to carbon deprivation: control by the supply of mitochondria with respiratory substrates. J Cell Biol 133:1251–1263

    Article  CAS  PubMed  Google Scholar 

  • Avin-Wittenberg T (2019) Autophagy and its role in plant abiotic stress management. Plant Cell Environ 42:1045–1053

    Article  CAS  PubMed  Google Scholar 

  • Bao Y, Song WM, Wang PP et al (2020) COST1 regulates autophagy to control plant drought tolerance. P Natl Acad Sci USA 117:7482–7493

    Article  CAS  Google Scholar 

  • Bassham DC (2007) Plant autophagy–more than a starvation response. Curr Opin Plant Biol 10:587–593

    Article  CAS  PubMed  Google Scholar 

  • Benchoam D, Cuevasanta E, Möller MN et al (2019) Hydrogen sulfide and persulfides oxidation by biologically relevant oxidizing species. Antioxidants (Basel) 8:48. https://doi.org/10.3390/antiox8020048

    Article  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  CAS  PubMed  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 

  • Chen J, Wu FH, Wang WH et al (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen SS, Jia HL, Wang XF et al (2020a) Hydrogen sulfide positively regulates abscisic acid signaling through persulfidation of SnRK2.6 in guard cells. Mol Plant 13:732–744

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Tian MM, Han Y (2020b) Hydrogen sulfide: a multi-tasking signal molecule in the regulation of oxidative stress responses. J Exp Bot 71:2862–2869

    Article  CAS  PubMed  Google Scholar 

  • Cheng TL, Shi JS, Dong YN et al (2018) Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage. Plant Growth Regul 84:11–23

    Article  CAS  Google Scholar 

  • Chung T, Suttangkakul A, Vierstra RD (2009) The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8- lipid adduct are regulated by development and nutrient availability. Plant Physiol 149:220–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark D, Durner J, Navarre DA et al (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1380–1384

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Barroso JB, González-Gordo S et al (2019a) Hydrogen sulfide: a novel component in Arabidopsis peroxisomes which triggers catalase inhibition. J Integr Plant Biol 61:871–883

    CAS  PubMed  Google Scholar 

  • Corpas FJ, González-Gordo S, Cañas A et al (2019b) Nitric oxide and hydrogen sulfide in plants: which comes first? J Exp Bot 70:4391–4404

    Article  CAS  PubMed  Google Scholar 

  • Cuevasanta E, Lange M, Bonanata J et al (2015) Reaction of hydrogen sulfide with disulfide and sulfenic acid to form the strongly nucleophilic persulfide. J Biol Chem 290:26866–26880

    Google Scholar 

  • de Pinto MC, Locato V, Sgobba A et al (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco bright Yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deng Y, Wang C, Wang N et al (2019) Roles of small-molecule compounds in plant adventitious root development. Biomol Ther 9:E420

    Google Scholar 

  • Doelling JH, Walker JM, Friedman EM et al (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 277:33105–33114

    Article  CAS  PubMed  Google Scholar 

  • Dóka É, Pader I, Bíró A et al (2016) A novel persulfide detection method reveals protein persulfide- and polysulfide-reducing functions of thioredoxin and glutathione systems. Sci Adv 2:e1500968

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dooley FD, Nair SP, Ward PD (2013) Increased growth and germination success in plants following hydrogen sulfide administration. PLoS One 8:e62048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du XZ, Jin ZP, Zhang LP et al (2019) H2S is involved in ABA-mediated stomatal movement through MPK4 to alleviate drought stress in Arabidopsis thaliana. Plant Soil 435:295–307

    Article  CAS  Google Scholar 

  • Fancy NN, Bahlmann A, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472

    Article  CAS  PubMed  Google Scholar 

  • Fang T, Cao Z, Li J et al (2014) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51

    Article  CAS  PubMed  Google Scholar 

  • Fang HH, Liu ZQ, Jin ZP et al (2016) An emphasis of hydrogen sulfide-cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis. Environ Pollut 213:870–877

    Article  CAS  PubMed  Google Scholar 

  • Fang HH, Liu ZQ, Long YP et al (2017) The Ca2+/calmodulin2-binding transcription factor TGA3 elevates LCD expression and H2S production to bolster Cr6+ tolerance in Arabidopsis. Plant J 91:1038–1050

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff NV, Battisti DS, Beachy RN et al (2010) Radically rethinking agriculture for the 21st century. Sci 327:833–834

    Article  CAS  Google Scholar 

  • Filipovic MR, Jovanovic VM (2017) More than just an intermediate: hydrogen sulfide signalling in plants. J Exp Bot 68:4733–4736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filipovic MR, Zivanovic J, Alvarez B et al (2018) Chemical biology of H2S signaling through persulfidation. Chem Rev 118:1253–1337

    Article  CAS  PubMed  Google Scholar 

  • Francoleon NE, Carrington SJ, Fukuto JM (2011) The reaction of H(2)S with oxidized thiols: generation of persulfides and implications to H(2)S biology. Arch Biochem Biophys 516:146–153

    Article  CAS  PubMed  Google Scholar 

  • Gao XH, Krokowski D, Guan BJ et al (2015) Quantitative HS-mediated protein sulfhydration reveals metabolic reprogramming during the integrated stress response. elife 4:e10067

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiger D, Scherzer S, Mumm P et al (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. P Natl Acad Sci USA 106:21425–21430

    Article  CAS  Google Scholar 

  • Gotor C, Garcia I, Aroca A et al (2019) Signaling by hydrogen sulfide and cyanide through post-translational modification. J Exp Bot 70:4251–4265

    Article  CAS  PubMed  Google Scholar 

  • Gudesblat GE, Iusem ND, Morris PC (2007) Guard cell-specific inhibition of Arabidopsis MPK3 expression causes abnormal stomatal responses to abscisic acid and hydrogen peroxide. New Phytol 173:713–721

    Article  CAS  PubMed  Google Scholar 

  • Guiboileau A, Avila-Ospina L, Yoshimoto K et al (2013) Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytol 199:683–694

    Article  CAS  PubMed  Google Scholar 

  • Han SJ, Yu BJ, Wang Y et al (2011) Role of plant autophagy in stress response. Protein Cell 2:784–791

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanaoka H, Noda T, Shirano Y et al (2002) Leaf senescence and starvation induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129:1181–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatzfeld Y, Maruyama A, Schmidt A et al (2000) Beta-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis. Plant Physiol 123:1163–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heppner DE, Hristova M, Ida T et al (2018) Cysteine perthiosulfenic acid (Cys-SSOH): a novel intermediate in thiol-based redox signaling? Redox Biol 14:379–385

    Article  CAS  PubMed  Google Scholar 

  • Herman EM, Baumgarther B, Chrispeels MJ (1981) Uptake and apparent digestion of cytoplasmic organelles by protein bodies (protein storage vacuoles) in mung bean cotyledons. Eur J Cell Biol 24:226–235

    CAS  PubMed  Google Scholar 

  • Huang D, Huo J, Zhang J et al (2019) Protein S-nitrosylation in programmed cell death in plants. Cell Mol Life Sci 76:1877–1887

    Google Scholar 

  • Huo J, Huang D, Zhang J et al (2018) Hydrogen sulfide: a gaseous molecule in postharvest freshness. Front Plant Sci 9:1172

    Article  PubMed  PubMed Central  Google Scholar 

  • Inoue Y, Suzuki T, Hattori M et al (2006) AtATG genes, homologs of yeast autophagy genes, are involved in constitutive autophagy in Arabidopsis root tip cells. Plant Cell Physiol 47:1641–1652

    Article  CAS  PubMed  Google Scholar 

  • Janse van Rensburg HC, Van den Ende W, Signorelli S (2019) Autophagy in plants: both a puppet and a puppet master of sugars. Front Plant Sci 10:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Jia H, Chen S, Liu D et al (2018) Ethylene-induced hydrogen sulfide negatively regulates ethylene biosynthesis by persulfidation of ACO in tomato under osmotic stress. Front Plant Sci 9:1517

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin Z, Wang Z, Ma Q et al (2017) Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana. Plant Soil 419:141–152

    Article  CAS  Google Scholar 

  • Khan MN, Mobin M, Abbas ZK et al (2017) Nitric oxide-induced synthesis of hydrogen sulfide alleviates osmotic stress in wheat seedlings through sustaining antioxidant enzymes, osmolyte accumulation and cysteine homeostasis. Nitric Oxide 68:91–102

    Article  CAS  PubMed  Google Scholar 

  • Khan MN, AlZuaibr FM, Al-Huqail AA et al (2018) Hydrogen sulfide-mediated activation of o-acetylserine (thiol) lyase and L/D-cysteine desulfhydrase enhance dehydration tolerance in Eruca sativa Mill. Int J Mol Sci 19:3981. https://doi.org/10.3390/ijms19123981

    Article  PubMed Central  Google Scholar 

  • Khan MN, Siddiqui MH, AlSolami MA et al (2020) Crosstalk of hydrogen sulfide and nitric oxide requires calcium to mitigate impaired photosynthesis under cadmium stress by activating defense mechanisms in Vigna radiata. Plant Physiol Biochem 156:278–290

    Article  CAS  PubMed  Google Scholar 

  • Klionsky DJ, Ohsumi Y (1999) Vacuolar import of proteins and organelles from the cytoplasm. Annu Rev Cell Dev Biol 15:1–32

    Article  CAS  PubMed  Google Scholar 

  • Krishnan N, Fu C, Pappin DJ et al (2011) H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci Signal 4:86

    Article  CAS  Google Scholar 

  • Lai DW, Mao Y, Zhou H et al (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 

  • Laureano-Marín AM, Moreno I, Romero LC et al (2016) Negative regulation of autophagy by sulfide is independent of reactive oxygen species. Plant Physiol 171:1378–1391

    PubMed  PubMed Central  Google Scholar 

  • Laureano-Marín AM, Aroca A, Perez-Perez ME et al (2020) Abscisic acid-triggered persulfidation of cysteine protease ATG4 mediates regulation of autophagy by sulfide. Plant Cell. https://doi.org/10.1105/tpc.20.00766

  • Li ZG, Yang SZ, Long WB et al (2013) 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 

  • Li ZG, Luo LJ, Zhu LP (2014) Involvement of trehalose in hydrogen sulfide donor sodium hydrosulfide-induced the acquisition of heat tolerance in maize (Zea mays L.) seedlings. Bot Stud 55:20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Q, Wang Z, Zhao Y et al (2016) Putrescine protects hulless barley from damage due to UV-B stress via H2S- and H2O2-mediated signaling pathways. Plant Cell Rep 35:1155–1168

    Article  CAS  PubMed  Google Scholar 

  • Li JS, Chen SS, Wang XF et al (2018) Hydrogen sulfide disturbs actin polymerization via S-sulfhydration resulting in stunted root hair growth. Plant Physiol 178:936–949

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li Z, Zhu Y, He X et al (2019) The hydrogen sulfide, a downstream signaling molecule of hydrogen peroxide and nitric oxide, involves spermidine-regulated transcription factors and antioxidant defense in white clover in response to dehydration. Environ Exp Bot 161:255–264

    Article  CAS  Google Scholar 

  • Lindermayr C, Sell S, Muller B et al (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lisjak M, Srivastava N, Teklic T et al (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 

  • Liu ZQ, Li YW, Cao CY et al (2019) The role of H2S in low temperature-induced cucurbitacin C increases in cucumber. Plant Mol Biol 99:535–544

    Article  CAS  PubMed  Google Scholar 

  • Ma DY, Ding HN, Wang CY et al (2016) Alleviation of drought stress by hydrogen sulfideIs partially related to the abscisic acid signaling pathway in wheat. PloS One 11:e0163082v

    Article  CAS  Google Scholar 

  • Marshall RS, Vierstra RD (2018) Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69:173–208

    Article  CAS  PubMed  Google Scholar 

  • Mei YD, Chen HT, Shen WB et al (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mostofa MG, Rahman A, Ansary MM et al (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz-Vargas MA, González-Gordo S, Cañas A et al (2018) Endogenous hydrogen sulfide (H2S) is up-regulated during sweet pepper (Capsicum annuum L.) fruit ripening. In vitro analysis shows that NADP-dependent isocitrate dehydrogenase (ICDH) activity is inhibited by H2S and nitric oxide. Nitric Oxide 81:36–45

    Article  PubMed  CAS  Google Scholar 

  • Muñoz-Vargas MA, González-Gordo S, Palma JM et al (2020) Inhibition of NADP-malic enzyme activity by H2S and NO in sweet pepper (Capsicum annuum L.) fruits. Physiol Plant 168:278–288

    PubMed  Google Scholar 

  • Mustafa AK, Gadalla MM, Sen N et al (2009) H2S signals through protein S-sulfhydration. Sci Signal 2:72

    Article  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S et al (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Ozfidan-Konakci C, Yildiztugay E, Elbasan F et al (2020) Hydrogen sulfide (HS) and nitric oxide (NO) alleviate cobalt toxicity in wheat (Triticum aestivum L.) by modulating photosynthesis, chloroplastic redox and antioxidant capacity. J Hazard Mater 388:122061

    Article  CAS  PubMed  Google Scholar 

  • Palma JM, Mateos RM, López-Jaramillo J et al (2020) Plant catalases as NO and HS targets. Redox Biol 34:101525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan J, Carroll KS (2013) Persulfide reactivity in the detection of protein S-sulfhydration. ACS Chem Biol 8:1110–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325e2336

    Article  CAS  Google Scholar 

  • Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev 113:4633–4679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian P, Sun R, Ali B et al (2014) Effects of hydrogen sulfide on growth, antioxidative capacity, and ultrastructural changes in oilseed rape seedlings under aluminum toxicity. J Plant Growth Regul 33:526–538

    Article  CAS  Google Scholar 

  • Ren X, Zou L, Zhang X et al (2017) Redox signaling mediated by thioredoxin and glutathione systems in the central nervous system. Antioxid Redox Signal 27:989–1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richau KH, Kaschani F, Verdoes M et al (2012) Subclassification and biochemical analysis of plant papain-like cysteine proteases displays subfamily-specific characteristics. Plant Physiol 158:1583–1599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson DG, Galili G, Herman E et al (1998) Topical aspects of vacuolar protein transport: autophagy and prevacuolar compartments. J Exp Bot 49:1263–1270

    Article  CAS  Google Scholar 

  • Sawahata T, Neal RA (1982) Use of 1-fluoro-2,4-dinitrobenzene as a probe for the presence of hydrodisulfide groups in proteins. Anal Biochem 126:360–364

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001a) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JI, Alllen GJ, Hugouvieux V et al (2001b) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658

    Article  CAS  PubMed  Google Scholar 

  • Scuffi D, Alvarez C, Laspina Net al. (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  PubMed Central  CAS  Google Scholar 

  • Scuffi D, Nietzel T, Di Fino LM et al (2018) Hydrogen sulfide increases production of NADPH oxidase-dependent hydrogen peroxide and phospholipase D-derived phosphatidic acid in guard cell signaling. Plant Physiol 176:2532–2542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sell S, Lindermayr C, Jörg D (2008) Identification of S-nitrosylated proteins in plants. Methods Enzymol 440:283–293

    Article  CAS  PubMed  Google Scholar 

  • Sen N, Paul BD, Gadalla MM et al (2012) Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions. Mol Cell 45:13–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen J, Zhang J, Zhou MJ et al (2020) Persulfidation-based modification of cysteine desulfhydrase and the NADPH oxidase RBOHD controls guard cell abscisic acid signaling. Plant Cell 32:1000–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sláviková S, Shy G, Yao Y et al (2005) The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J Exp Bot 56:2839–2849

    Article  PubMed  Google Scholar 

  • Swanson SJ, Bethke PC, Jones RL (1998) Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes. Plant Cell 10:685–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M et al (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184

    Article  CAS  PubMed  Google Scholar 

  • Toyooka K, Okamoto T, Minamikawa T (2001) Cotyledon cells of Vigna mungo seedlings use at least two distinct autophagic machineries for degradation of starch granules and cellular components. J Cell Biol 154:973–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandiver M, Snyder S (2012) Hydrogen sulfide: a gasotransmitter of clinical relevance. J Mol Med 90:255–263

    Article  CAS  PubMed  Google Scholar 

  • Vandiver MS, Paul BD, Xu R et al (2013) Sulfhydration mediates neuroprotective actions of parkin. Nat Commun 4:1626

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li L, Cui W et al (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 P, Du Y, Hou YJ et al (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci 112:613–618

    Article  CAS  PubMed  Google Scholar 

  • Wedmann R, Onderka C, Wei S et al (2016) Improved tag-switch method reveals that thioredoxin acts as depersulfidase and controls the intracellular levels of protein persulfidation. Chem Sci 7:3414–3426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie Y, Zhang C, Lai D et al (2014) 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  CAS  PubMed  Google Scholar 

  • Yamaguchi Y, Nakamura T, Kusano T et al (2000) Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41:465–476

    Article  CAS  PubMed  Google Scholar 

  • Yang GD, Wu LY, Jiang B et al (2008) H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322:587–590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang HJ, Mu JY, Chen LC et al (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F, Xie Q (2017) Non-26S proteasome endomembrane trafficking pathways in ABA signaling. Trends Plant Sci 22:976–985

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Feechan A, Yin MH et al (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Zhou MJ, Ge ZL et al (2020) Abscisic acid-triggered guard cell L-cysteine desulfhydrase function and in situ hydrogen sulfide production contributes to heme oxygenase-modulated stomatal closure. Plant Cell Environ 43:624–636

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang X, Cui Y, Gao C et al (2015) Endocytic and autophagic pathways crosstalk in plants. Curr Opin Plant Biol 28:39–47

    Article  CAS  PubMed  Google Scholar 

  • Ziogas V, Molassiotis A, Fotopoulos V et al (2018) Hydrogen sulfide: a potent tool in postharvest fruit biology and possible mechanism of action. Front Plant Sci 9:1375

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 32072559, 31860568, 31560563 and 31160398); the Research Fund of Higher Education of Gansu, China (No. 2018C-14); the Natural Science Foundation of Gansu Province, China (Nos. 1606RJZA073, 1606RJZA077 and 1606RJYA252).

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Huang, D., Li, C., Wang, C., Liao, W. (2021). Hydrogen Sulfide and Posttranslational Modification of Proteins: A Defense Strategy Against Abiotic Stress. In: Khan, M.N., Siddiqui, M.H., Alamri, S., Corpas, F.J. (eds) Hydrogen Sulfide and Plant Acclimation to Abiotic Stresses. Plant in Challenging Environments, vol 1. Springer, Cham. https://doi.org/10.1007/978-3-030-73678-1_12

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