Advertisement

Interaction between hydrogen sulfide and hormones in plant physiological responses

  • Huyi He
  • Carlos Garcia-Mata
  • Long-Fei HeEmail author
Review paper

Abstract

The gasotransmitter, hydrogen sulfide (H2S) is involved in plant growth and development, and stress responses. Plant hormones influence the levels of endogenous H2S and H2S may affect the biosynthesis, transport, and signal transduction of different phytohormones. The dual role of H2S in the interaction with phytohormones contributes to the physiological functions of H2S in the life cycle and responses to abiotic stresses in plants. The biological effect of H2S might depend on the ratio between phytohormones. However, the mechanism by which H2S and plant hormones interplay in plants remains fragmentary. This review summarized the biosynthesis and degradation of H2S and discussed the cross-talk between H2S and different phytohormones along with the future perspectives.

Keywords

Hydrogen sulfide Plant hormone Interaction Transcription factor Plant 

Abbreviations

ABA

Abscisic acid

ACC

1-Aminocyclopropane 1-carboxylic acid

ACO

ACC oxidase

ACS

ACC synthase

ATFs

AP2-domain-containing transcription factors

Ca

Calcium

CA

Carbonic anhydrase

CAS

Cyanoalanine synthase

Cd

Cadimum

CDes

Cysteine desulfhydrases

CDPK

Calcium-dependent protein kinase

CO

Carbon monoxide

COS

Carbonyl sulfide

Cu

Copper

DCD

d-Cysteine desulfhydrase

DES

l-Cys desulfhydrase

ET

Ethylene

EUI

Elongated uppermost internode

GA

Gibberellin

GA2ox

GA2-oxidase

HO

Heme oxidase

H2S

Hydrogen sulfide

HT

Hypotaurine

IAA

Indole-3-acetic acid

JA

Jasmonic acid

JAZ

JASMONATE ZIM-domain

LCD

l-Cysteine desulfhydrase

NCED

9-cis-Epoxycarotenoid dioxygenase

NaHS

Sodium hydrosulfide

NFS

Nitrogenase Fe–S cluster

NO

Nitric oxide

NPA

N-1-naphthylphthalamic acid

OAS-TL

O-acetyl-l-serine(thiol)lyase

PCD

Programmed cell death

SA

Salicylic acid

SiR

Sulfite reductase

Notes

Acknowledgements

This study was supported by Grants from the National Natural Science Foundation of China (No. 31660352), the Science & Technology Development Fund of Guangxi Academy of Agricultural Sciences (Guinongke2017JZ11 and Guinongke2017JZ21), and Natural Science Foundation of Guangxi (2015GXNSFAA139079). We thank the reviewers for their helpful comments on this manuscript.

References

  1. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16:1066–1071PubMedCrossRefGoogle Scholar
  2. Al Ubeed HMS, Wills RBH, Bowyer MC, Vuong QV, Golding JB (2017) Interaction of exogenous hydrogen sulphide and ethylene on senescence of green leafy vegetables. Postharvest Biol Technol 133:81–87CrossRefGoogle Scholar
  3. Ali B, Mwamba TM, Gill RA, Yang C, Ali S, Daud MK, Wu Y, Zhou W (2014) Improvement of element uptake and antioxidative defense in Brassica napus under lead stress by application of hydrogen sulfide. Plant Growth Regul 74:261–273CrossRefGoogle Scholar
  4. Alvarez C, Calo L, Romero LC, Garcia I, Gotor C (2010) An O-Acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 152:656–669PubMedCrossRefPubMedCentralGoogle Scholar
  5. Alvarez C, Garcia I, Romero LC, Gotor C (2012) Mitochondrial sulfide detoxification requires a funtional isoform O-acetylserine(thiol)lyase C in Arabidopsis thaliana. Mol Plant 5:1217–1226PubMedCrossRefGoogle Scholar
  6. Aroca A, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine posttranslational modification in plant systems. Plant Physiol 168:334–342PubMedCrossRefPubMedCentralGoogle Scholar
  7. Aroca A, Benito JM, Gotor C, Romero LC (2017) Persulfidation proteome reveals the regulation of protein function by hydrogen sulfide in diverse biological processes in Arabidopsis. J Exp Bot 68:4915–4927PubMedCrossRefPubMedCentralGoogle Scholar
  8. Banerjee A, Tripathi DK, Roychoudhury A (2018) Hydrogen sulphide trapeze: environmental stress amelioration and phytohormone crosstalk. Plant Physiol Biochem.  https://doi.org/10.1016/j.plaphy.2018.08.028 CrossRefPubMedGoogle Scholar
  9. Barry CS, LIop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol 123:979–986PubMedCrossRefPubMedCentralGoogle Scholar
  10. Baudouin E, Poilevey A, Indiketi Hewage N, Cochet F, Puyaubert J, Bailly C (2016) The significance of hydrogen sulfide for Arabidopsis seed germination. Front Plant Sci 7:930PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bloem E, Riemenschneider A, Volker J, Papenbrock J, Schmidt A, Salac I, Haneklaus S, Schnug E (2004) Sulphur supply and infection with Pyrenopeziza brassicae influence l-cysteine desulphydrase activity in Brassica napus L. J Exp Bot 55:2305–2312PubMedCrossRefPubMedCentralGoogle Scholar
  12. Che YM, Hou LX, Sun YJ, Liu X (2016) Hydrogen sulfide functions in regulation of stomatal movement and stress response in plant. Biotechnol Bull 32:18–26. (in Chinese)Google Scholar
  13. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol 154:810–819PubMedCrossRefPubMedCentralGoogle Scholar
  14. 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 362:301–318CrossRefGoogle Scholar
  15. Chen J, Wu FH, Shang YT, Wang WH, Hu WJ, Simon M, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J Exp Bot 66:6605–6622PubMedCrossRefPubMedCentralGoogle Scholar
  16. Cheng T, Shi J, Dong Y, Ma Y, Peng Y, Hu X, Chen J (2018) Hydrogen sulfide enhances poplar toelrance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen species. Plant Growth Regul 84:11–23CrossRefGoogle Scholar
  17. Christou A, Manganaris GA, Papadopoulos I, Fotopoulos V (2013) Hydrogen sulfide induces systemic tolerance to salinity and non-ionic osmotic stress in strawberry plants through modification of reactive species biosynthesis and transcriptional regulation of multiple defence pathways. J Exp Bot 64:1953–1966PubMedCrossRefPubMedCentralGoogle Scholar
  18. Deng YQ, Bao J, Yuan F, Liang X, Feng ZT, Wang BS (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content. Plant Growth Regul 79:391–399CrossRefGoogle Scholar
  19. Duan B, Ma Y, Jiang M, Yang F, Ni L, Lu W (2015) Improvement of photosynthesis in rice (Oryza sativa L.) as a result of an increase in stomatal aperture and density by exogenous hydrogen sulfide treatment. Plant Growth Regul 75:33–44CrossRefGoogle Scholar
  20. Fang HH, Jing T, Liu ZQ, Zhang L, Jin Z, Pen Y (2014a) Hydrogen sulfide interacts with calcium signaling to enhancethe chromium tolerance in Setaria italica. Cell Calcium 56:472–481PubMedCrossRefPubMedCentralGoogle Scholar
  21. Fang T, Cao Z, Li J, Shen W, Huang L (2014b) Auxin-induced hydrogen sulfide generation is involved in lateral root formation in tomato. Plant Physiol Biochem 76:44–51PubMedCrossRefPubMedCentralGoogle Scholar
  22. Fang H, Liu Z, Long Y, Liang Y, Jin Z, Zhang L, Liu D, Li H, Zhai J, Pei Y (2017) The Ca2+/calmodulin2-binding transcription factor TGA3 elevates LCD expression and H2S production to bolster Cr6+ tolerance in Arabidopsis. Plant J 91:1038–1050PubMedCrossRefPubMedCentralGoogle Scholar
  23. Filipovic MR, Jovanovic VM (2017) More than just an intermediate: hydrogen sulfide signalling in plants. J Exp Bot 68:4733–4736PubMedCrossRefPubMedCentralGoogle Scholar
  24. Garcia MJ, Lucena C, Romera FJ, Alcantara E, Perez-Vicente R (2010) Ethylene and nitric oxide involvedment in the up-regulation of key genes related to iron acquisition and homestasis in Arabidopsis. J Exp Bot 61:3885–3899PubMedCrossRefPubMedCentralGoogle Scholar
  25. Garcia MJ, Suarez V, Romera FJ, Alcantara E, Perez-Vicente R (2011) A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in strategy I plants. Plant Physiol Biochem 49:537–544PubMedCrossRefPubMedCentralGoogle Scholar
  26. Garcia-Mata C, Lamattina L (2010) Hydrogen sulphide, a novel gasotransmitter involved in guard cell signaling. New Phytol 188:977–984PubMedCrossRefPubMedCentralGoogle Scholar
  27. Hancock JT (2018) Hydrogen sulfide and environmental stresses. Environ Exp Bot.  https://doi.org/10.1016/j.envexpbot.2018.08.034 CrossRefGoogle Scholar
  28. Hancock JT, Whiteman M (2014) Hydrogen sulfide and cell signaling: team player or referee? Plant Physiol Biochem 78:37–42PubMedCrossRefPubMedCentralGoogle Scholar
  29. Harrington HM, Smith IK (1980) Cysteine metabolism in cultured tobacco cells. Plant Physiol 65:151–155PubMedCrossRefPubMedCentralGoogle Scholar
  30. He H, He L, Gu M (2012a) Interactions between nitric oxide and plant hormones in aluminum tolerance. Plant Signal Behav 7:469–471PubMedCrossRefPubMedCentralGoogle Scholar
  31. He HY, He LF, Gu MH, Li XF (2012b) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130PubMedCrossRefPubMedCentralGoogle Scholar
  32. Honda K, Yamada N, Yoshida R, Ihara H, Sawa T, Akaike T, Iwai S (2015) 8-Mercapto-cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis. Plant Cell Physiol 56:1481–1489PubMedCrossRefPubMedCentralGoogle Scholar
  33. 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 6:396–406. (in Chinese)Google Scholar
  34. Hou ZH, Wang LX, Liu J, Hou L, Liu X (2013) Hydrogen sulfide regulates ethylene-induced stomatal closure in Arabidopsis thaliana. J Integr Plant Biol 55:277–289PubMedCrossRefPubMedCentralGoogle Scholar
  35. Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormone. J Exp Bot 68:1361–1369PubMedCrossRefPubMedCentralGoogle Scholar
  36. Huang H, Liu B, Liu L, Song S (2017) Jasmonate action in plant growth and development. J Exp Bot 68:1349–1359PubMedCrossRefPubMedCentralGoogle Scholar
  37. Jia H, Hu Y, Fan T, Li J (2015) Hydrogen sulfide modulates actin-dependent auxin transport via regulating ABPs results in changing of root development in Arabidopsis. Sci Rep 5:8251PubMedCrossRefPubMedCentralGoogle Scholar
  38. Jin ZP, Pei YX (2015) Physiological implications of hydrogen sulfide in plants: pleasant exploration behind its unpleasant odour. Oxid Med Cell Longev 2015:1–6Google Scholar
  39. Jin ZP, Pei Y (2016) Hydrogen sulfide: the shutter button of stomata in plants. Sci China Life Sci 59:1187–1188PubMedCrossRefPubMedCentralGoogle Scholar
  40. Jin CW, Du ST, Shamsi IH, Luo BF, Lin XY (2011a) NO synthase-generated NO acts downstream of auxin in regulating Fe-deficiency-induced root branching that enhances Fe-deficiency tolerance in tomato plants. J Exp Bot 62:3875–3884PubMedCrossRefPubMedCentralGoogle Scholar
  41. Jin ZP, Shen JJ, Qiao ZJ, Yang GD, Wang R, Pei YX (2011b) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Commun 414:481–486PubMedCrossRefPubMedCentralGoogle Scholar
  42. Jin ZP, Xue SW, Luo YN, Tian BH, Fang HH, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46PubMedCrossRefPubMedCentralGoogle Scholar
  43. Jin ZP, Wang Z, Ma Q, Sun L, Zhang L, Liu Z, Liu D, Hao X, Pei Y (2017) Hydrogen sulfide mediates ion fluxes inducing stomatal closure in response to drought stress in Arabidopsis thaliana. Plant Soil 419:141–152CrossRefGoogle Scholar
  44. Kushnir S, Babiychuk E, Storozhenko S, Davey MW, Papenbrock J, De Rycke R, Engler G, Stephan UW, Lange H, Kispal G, Lill R, Montagu M (2001) A mutation of the mitochondrial ABC transporter Sta1 leads to dwarfism and chlorosis in the Arabidopsis mutant starik. Plant Cell 13:89–100PubMedCrossRefPubMedCentralGoogle Scholar
  45. Lamattina L, Garcia-Mata C (2016) Gasotransmitters in plants, signaling and communication in plants. Springer, Switzerland, pp 23–51CrossRefGoogle Scholar
  46. Leon S, Tournaine B, Briat JF, Lobreaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a Nifs-like plastidial cysteine desulphurase. Biochem J 366:557–564PubMedCrossRefPubMedCentralGoogle Scholar
  47. Li ZG, Gong M, Xie H, Yang L, Li J (2012) Hydrogen sulfide donor sodium hydrosulfide-induced heat toelrance in tobacco (Nicotiana tabacum L.) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185:185–189PubMedCrossRefPubMedCentralGoogle Scholar
  48. Li YJ, Shi ZQ, Gan LJ, Chen J (2014) Hydrogen sulfide is a novel gasotransmitter with pivotal role in regulating lateral root formation in plants. Plant Signal Behav 9:e29127PubMedCrossRefPubMedCentralGoogle Scholar
  49. Li ZG, Xie LR, Li XJ (2015a) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127PubMedCrossRefPubMedCentralGoogle Scholar
  50. Li ZG, Long WB, Yang SZ, Wang YC, Tang JH, Wen L, Zhu BY, Min X (2015b) Endogenous hydrogen sulfide regualted by calcium is involved in thermotolerance in tobacco Nicotiana tabacum L. suspension cell cultures. Acta Physiol Plant 37:1–11CrossRefGoogle Scholar
  51. Lin VS, Chang CJ (2012) Fluorescent probes for sensing and imaging biological hydrogen sulfide. Curr Opin Chem Biol 16:1–7CrossRefGoogle Scholar
  52. 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 31:519–528CrossRefGoogle Scholar
  53. 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 48:931–935PubMedCrossRefPubMedCentralGoogle Scholar
  54. Lisjak M, Teklic T, Wilson ID, Wood M, Whiteman M, Hancock JT (2011) Hydrogen sulfide effects on stomatal apertures. Plant Signal Behav 10:1444–1446CrossRefGoogle Scholar
  55. Lisjak M, Teklic T, Wilson ID, Whiteman M, Hancock JT (2013) Hydrogen sulfide: environmental factor or signalling molecule? Plant Cell Environ 36:1607–1616PubMedCrossRefPubMedCentralGoogle Scholar
  56. Liu J, Hou ZH, Zhao FG, Liu X (2011a) Hydrogen sulfide mediates ABA-induced stomatal closure of Vicia faba L. Acta Bot Boreal-Occident Sin 31:298–304. (in Chinese)Google Scholar
  57. Liu J, Hou LX, Liu GH, Liu X, Wang XC (2011b) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56:3547–3553CrossRefGoogle Scholar
  58. Liu J, Hou ZH, Liu GH, Hou L, Liu X (2012) Hydrogen sulfide may function downstream of nitric oxide in ethylene induced stomatal closure in Vicia faba L. J Integr Agr 11:1644–1653CrossRefGoogle Scholar
  59. Liu Z, Fang H, Pei Y, Jin Z, Zhang L, Liu D (2015) WRKY transcription factors down-regulate the expression of H2S-generating genes, LCD and DES in Arabidopsis thaliana. Sci Bull 60:995–1001CrossRefGoogle Scholar
  60. Liu X, Chen J, Wang GH, Wang WH, Shen ZJ, Luo MR, Gao GF, Simon M, Ghoto K, Zheng HL (2016) Hydrogen sulfide alleviates zinc toxicity by reducing zinc uptake and regualting genes expressions of antioxidative enzymes and metallothioneins in roots of the cadmium/zinc hyperaccumulator Solanum nigrum L. Plant Soil 400:177–192CrossRefGoogle Scholar
  61. Mur LAJ, Laarhoven LJJ, Harren FJM, Hall MA, Smith AR (2008) Nitric oxide interacts with salicylate to regulate biphasic ethylene production during the hypersensitive response. Plant Physiol 148:1537–1546PubMedCrossRefPubMedCentralGoogle Scholar
  62. Pandey S (2014) Hydrogen sulfide: a new node in the acscisic acid-dependent guard cell signaling network? Plant Physiol 166:1680–1681PubMedCrossRefPubMedCentralGoogle Scholar
  63. Papanatsiou M, Scuffi D, Blatt MR, García-Mata C (2015) Hydrogen sulfide regulates inward-rectifying K+ channels in conjunction with stomatal closure. Plant Physiol 168:29–35PubMedCrossRefPubMedCentralGoogle Scholar
  64. 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 (Stuttg) 9:582–588CrossRefGoogle Scholar
  65. Paul BD, Snyder SH (2012) H2S signalling through protein sulfhydration and beyond. Nat Rev Mol Cell Biol 13:499–507PubMedCrossRefPubMedCentralGoogle Scholar
  66. Peng RY, Bian ZY, Zhou LN, Cheng W, Hai N, Yang CQ, Yang T, Wang XY, Wang CY (2016) Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). Plant Cell Rep 35:2325–2340PubMedCrossRefPubMedCentralGoogle Scholar
  67. Qiao ZJ, Jing T, Liu ZQ, Zhang L, Jin Z, Liu D, Pei Y (2015) H2S acting as a downstream signaling molecule of SA regulates Cd tolerance in Arabidopsis. Plant Soil 393(1–2):137–146CrossRefGoogle Scholar
  68. Qiao ZJ, Jing T, Jin Z, Liang Y, Zhang L, Liu Z, Liu D, Pen Y (2016) CDPKs enhance Cd tolerance through intensifying H2S signal in Arabidopsis thaliana. Plant Soil 398:99–110CrossRefGoogle Scholar
  69. Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends Plant Sci 10:503–509PubMedCrossRefGoogle Scholar
  70. Riemenschneider A (2006) Isolation and characterization of cysteine-degrading and H2S-releasing enzymes of higher plants. PhD Thesis, University of HannoverGoogle Scholar
  71. Riemenschneider A, Bonacina E, Schmidt A, Papenbrock J (2005a) Remove from marked Records Isolation and characterization of a second d-cysteine desulfhydrase-like protein from Arabidopsis. In: Saito K, de Kok LJ, Stulen I, Hawkesford MJ, Schnug E, Sirko A, et al (eds) Sulfur transport and assimilation in plants in the Post Genomic Era. Papers from the 6th International Workshop on Plant Sulfur Metabolism, Chiba, Japan, pp 103–106Google Scholar
  72. Riemenschneider A, Nikiforova V, Hoefgen R, de Kok LJ, Papenbrock J (2005b) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483PubMedCrossRefGoogle Scholar
  73. Romero LC, Aroca MA, Laureano-Marin AM, Moreno I, Garcia I, Gotor C (2014) Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol Plant 7:264–276PubMedCrossRefGoogle Scholar
  74. Schmidt A (1982) A cysteine desulfhydrase from spinach leaves specific for D-cysteine. Z Pflanzenphysiol 107:301–312CrossRefGoogle Scholar
  75. Scuffi D, Alvarez C, Laspina N, Gotor C, Lamattina L, Garcia-Mata C, Sekiya J, Schmidt A, Wilson LG (2014) Hydrogen sulfide generated by l-Cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol 166:2065–2076PubMedCrossRefPubMedCentralGoogle Scholar
  76. Sekiya J, Schmidt A, Wilson LG (1982) Emission of hydrogen sulfide by leaf tissue in response to L-cysteine. Plant Physiol 70:430–436PubMedCrossRefPubMedCentralGoogle Scholar
  77. Shao R, Wang K, Shangguan Z (2010) Cytokinin-induced photosynthetic adaptability of Zea mays L. to drought stress associated with nitric oxide signal: probed bt ESR spectroscopy and fast OJIP fluorescence rise. J Plant Physiol 167:472–479PubMedCrossRefGoogle Scholar
  78. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of acscisic acid and gibberellins in Arabidopsis. PLoS Genet 9:e1003577PubMedCrossRefPubMedCentralGoogle Scholar
  79. Shu K, Zhou W, Yang W (2017) APETALA 2-domain-containing transcription factors: focusing on acscisic acid and gibberellins antagonism. New Phytol 1:1–7Google Scholar
  80. Sirko A, Blaszczyk A, Liszewska F (2004) Overproduction os SAT and OASTL in transgenic plants: a survey of effects. J Exp Bot 55:1881–1888PubMedCrossRefGoogle Scholar
  81. Soutourina J, Blanquet S, Plateau P (2001) Role of d-cysteine desulfhydrase in the adaptation of Escherichia coli to d-cysteine. J Biol Chem 276:40864–40872PubMedCrossRefGoogle Scholar
  82. Stimler K, Berry JA, Yakir D (2012) Effects of carboonyl sulfide and carbonic anhydrase on stomatal conductance. Plant Physiol 157:509–517CrossRefGoogle Scholar
  83. Tai CH, Cook PF (2000) O-acetylserine sulfhydrylase. Adv Enzymol Relat Areas Mol Biol 74:185–234PubMedGoogle Scholar
  84. Wang R (2012) Physiological implication of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896PubMedCrossRefGoogle Scholar
  85. Wang HH, Liang XL, Wan Q, Wang XM, Bi YR (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307CrossRefGoogle Scholar
  86. 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 351:107–119CrossRefGoogle Scholar
  87. Wang L, Wan R, Shi Y, Xue S (2016) Hydrogen sulfide activates S-type anion channel via OST1 and Ca2+ modules. Mol Plant 9:489–491PubMedCrossRefGoogle Scholar
  88. Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246PubMedCrossRefPubMedCentralGoogle Scholar
  89. Xie Y, Lai D, Mao Y, Zhang W, Shen W, Guan R (2013) Molecular cloning, characterization, and expression analysis of a novel gene encoding l-cysteine desulfhydrase from Brassica napus. Mol Biotechnol 54:737–746PubMedCrossRefPubMedCentralGoogle Scholar
  90. Xie YJ, Zhang C, Lai DW, Sun Y, Samma MK, Zhang J, Shen W (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 171:53–62PubMedCrossRefPubMedCentralGoogle Scholar
  91. Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330CrossRefGoogle Scholar
  92. Yaish MW, El-Kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interaction between abscisic acid and gibberellins in rice. PLoS Genet 6:e1001098PubMedCrossRefPubMedCentralGoogle Scholar
  93. Yamaguchi Y, Nakamura T, Kusano T, Sano H (2000) Three Arabidopsis genes encoding proteins with differential activities for cysteine synthase and beta-cyanoalanine synthase. Plant Cell Physiol 41:465–476PubMedCrossRefPubMedCentralGoogle Scholar
  94. Yu L, Shang H, Zhang C, Wang X, Wei M, Yang F, Shi Q (2011) Effects of exogenous H2S on the physiological and biochemical characteristics of the cucumber hypocotyls and radicles under cadmium stress. Acta Horticulturae Sinica 38:2131–2139. (in Chinese)Google Scholar
  95. 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 50:1518–1529PubMedCrossRefPubMedCentralGoogle Scholar
  96. Zhang H, Tang J, Liu XP, Wang Y, Yu W, Peng WY, Fang F, Ma DF, Wei ZJ, Hu LY (2009a) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094PubMedCrossRefPubMedCentralGoogle Scholar
  97. Zhang H, Ye YK, Wang SH, Luo JP, Tang J, Ma DF (2009b) Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul 58:243–250CrossRefGoogle Scholar
  98. Zhang H, Dou W, Jiang CX, Wei ZJ, Liu J, Jones RL (2010) Hydrogen sulfide stimulates β-amylase activity during early stages of wheat grain germination. Plant Signal Behav 5:1031–1033PubMedCrossRefPubMedCentralGoogle Scholar
  99. 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 Tec 60:251–257CrossRefGoogle Scholar
  100. Zhou ZH, Wang Y, Ye XY, Li ZG (2018) Signaling molecule hydrogen sulfide improves seed germination and seedling growth of maize (Zea mays L.) under high temperature by inducing antioxidant system and osmolyte biosynthesis. Front Plant Sci 9:1288PubMedCrossRefPubMedCentralGoogle Scholar
  101. Zhu XF, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ (2012) Gibberellinc acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of ITR1 in Arabidopsis thaliana. J Hazard Mater 239–240:302–307PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of AgronomyGuangxi UniversityNanningPeople’s Republic of China
  2. 2.Cash Crops Research InstituteGuangxi Academy of Agricultural SciencesNanningPeople’s Republic of China
  3. 3.Instituto de Investigaciones Biológicas, Universidad Nacional de Mar del Plata, Consejo Nacional de Investigaciones Científicas y Técnicas (IIB-UNMdP-CONICET)Mar del PlataArgentina

Personalised recommendations