Skip to main content

Advertisement

SpringerLink
Log in

Hydrogen Sulfide: A Novel Gaseous Molecule for Plant Adaptation to Stress

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Hydrogen sulfide (H2S) has emerged as a novel gaseous signal molecule with multifarious effects on seed germination, plant growth, development, and physiological processes. Due to its dominant role in plant stress tolerance and cross-adaptation, it is getting more attention nowadays, although it has been largely referred as toxic and environmental hazardous gas. In this review work, we are highlighting the importance of H2S as an essential gaseous molecule to help in signaling, metabolism, and stress tolerance in plants. Firstly, production of H2S from different natural and artificial sources were discussed with its transformation from sulfur (S) to sulfate (SO42−) and then to sulfite (SO32−). The importance of different kinds of transporters that helps to take SO42− from the soil solution was presented. Mainly, these transporters are SULTRs (H+/SO42− cotransporters) and multigene family encodes them. Furthermore, these SULTRs have LAST (Low affinity transport proteins), HAST (High affinity transport proteins), vacuole transporters, and plastid transporters. Since it is well known that there is strong relationship between SO42− and synthesis of hydrogen sulfide or dihydrogen sulfide or sulfane in plant cells. Thus, cysteine (Cys) metabolism through which H2S could be generated in plant cell with the role of different enzymes has been presented. Furthermore, H2S in interaction with other molecules could help to mitigate biotic and abiotic stress. Based on this review work, it can be concluded that H2S has potential to induce cross-adaptation to biotic and abiotic stress; thus, it is recommended that it should be considered in future studies to answer the questions like what are the receptors of H2S in plant cell, where in plants the physiological concentration of H2S is high in response to multiple stress and how it induces cross-adaptation by interaction with other signal molecules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CAS:

Cyano alanine synthase

CS:

Cysteine synthase

Cys:

Cysteine

DES1:

l-Cysteine Desulhydrase

DMS:

Dimethyl sulfide

HAST:

High affinity transport proteins

LAST:

Low affinity transport proteins

LCDSH/DCDSH:

l- and d-cysteine desulfhydrase

MAPK:

Mitogen-activated protein kinase

PTMs:

Persulfidation and S-nitrosation

SR:

Sulfite reductase

References

  • Aiuppa A, Inguaggiato S, McGonigle AJS, O’Dwyer M, Oppenheimer C, Padgett MJ, Rouwet D, Valenza M (2005) H2S fluxes from Mt. Etna, Stromboli, and Vulcano (Italy) and implications for the sulfur budget at volcanoes. Geochim Cosmochim Acta 69:1861–1871

    CAS  Google Scholar 

  • Akter N, Islam MR (2017) Heat stress effects and management in wheat. A review. Agron Sustain Dev 37:37

    Google Scholar 

  • 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 152:656–669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andreae MO (1990) Ocean-atmosphere interactions in the global biogeochemical sulfur cycle. Mar Chem 30:1–29

    CAS  Google Scholar 

  • Antoniou C, Xenofontos R, Chatzimichail G, Christou A, Kashfi K, Fotopoulos V (2020) Exploring the potential of nitric oxide and hydrogen sulfide (NOSH)-releasing synthetic compounds as novel priming agents against drought stress in Medicago sativa plants. Biomoleclues 10(1):E120

    Google Scholar 

  • Arnao MB, Hernandez-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59:133–150

    CAS  PubMed  Google Scholar 

  • Aroca Á, Serna A, Gotor C, Romero LC (2015) S-sulfhydration: a cysteine post-translational modification in plant systems. Plant Physiol 168:334–342

    CAS  PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Ausma T, De Kok LJ (2019) Atmospheric H2S: impact on plant functioning. Front Plant Sci 10:743

    PubMed  PubMed Central  Google Scholar 

  • Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MSA (2014a) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res 21:717–731

    CAS  Google Scholar 

  • Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MSA (2014b) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res 21(1):717–731

    CAS  Google Scholar 

  • Bhomick PC, Rao KS (2014) Sources and effects of hydrogen sulfide. J Appl Chem 3(3):914–918

    Google Scholar 

  • 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(406):2305–2312

    CAS  PubMed  Google Scholar 

  • Brace EC, Engelberth AS (2020) Assessing viability of soybean oils to remove hydrogen sulfide from natural gas. ACS Sustain Chem Eng 8:9377

    CAS  Google Scholar 

  • Cao M-J, Wang Z, Wirtz M, Hell R, Oliver DJ, Xiang C-B (2013) SULTR3;1 is a chloroplast-localized sulfate transporter in Arabidopsis thaliana. Plant J 73:607–616

    CAS  PubMed  Google Scholar 

  • Carter JM, Brown EM, Grace JP, Salem AK, Irish EE, Bowden NB (2018) Improved growth of pea, lettuce, and radish plants using the slow release of hydrogen sulfide from GYY-4137. PLoS ONE 13(12):e0208732

    PubMed  PubMed Central  Google Scholar 

  • Chao TT, Harward ME, Fang SC (1962) Adsorption and desorption phenomena of sulfate ions in soils. Soil Sci Soc Am J 26:234–237

    CAS  Google Scholar 

  • Chen J, Wu FH, Wang WH, Zheng CJ, Lin GH, Dong XJ, He JX, Pei ZM, Zheng HL (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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang W-H, Wu F-H, He E-M, Liu X, Shangguan Z-P, Zheng H-L (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Chen Q, Zhang X, Li R, Jia Y, Ef A, Jia A, Hu L, Hu H (2016) Hydrogen sulfide mediates nicotine biosynthesis in tobacco (Nicotiana tabacum) under high temperature conditions. Plant Physiol Biochem 104:174–179

    CAS  PubMed  Google Scholar 

  • Cheng W, Zhang L, Jiao C, Su M, Yang T, Zhou L, Peng R, Wang R, Wang C (2013) Hydrogen sulfide alleviates hypoxia-induced root tip death in Pisum sativum. Plant Physiol Biochem 70:278–286

    CAS  PubMed  Google Scholar 

  • Christou A, Manganaris GA, Papadopoulos I, Fotopouls 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 64:1953–1966

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    CAS  PubMed  Google Scholar 

  • Christou A, Manganaris G, Papadopoulos I, Fotopoulos V (2011) Hydrogen sulfide confers systemic tolerance to salt and polyethylene glycol stress in strawberry plants. In: Abstracts book of the 10th International Conference on Reactive Oxygen and Nitrogen Species in Plants, 5–8 July 2011, Budapest, Hungary, p 159

  • Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42

    PubMed  PubMed Central  Google Scholar 

  • Corpas FJ, Palma JM (2020) H2S signaling in plants and applications in agriculture. J Adv Res 24:131–137

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Kok LJ, Thompson CR, Kuiper PJC (1983) Sulfide-induced oxygen uptake by isolated spinach chloroplasts catalyzed by photosynthetic electron transport. Physiol Plant 59:19–22

    Google Scholar 

  • 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 79:391–399

    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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorman DC, Moulin FJ, McManus BE, Mahle KC, James RA, Struve MF (2002) 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

    CAS  PubMed  Google Scholar 

  • 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(1):33–44

    CAS  Google Scholar 

  • Fang H, Jing T, Liu Z, Zhang L, Jin Z, Pei Y (2014) Hydrogen sulfide interacts with calcium signaling to enhance the chromium tolerance in Setaria italica. Cell Calcium 56:472–481

    CAS  PubMed  Google Scholar 

  • Fang H, Liu Z, Jin Z, Zhang L, Liu D, Pei Y (2016) An emphasis of hydrogen sulfide-cysteine cycle on enhancing the tolerance to chromium stress in Arabidopsis. Environ Pollut 213:870–877

    CAS  PubMed  Google Scholar 

  • Filipovic MR, Jovanović VM (2017) More than just an intermediate: hydrogen sulfide signalling in plants. J Exp Bot 68(17):4733–4736

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fu PN, Wang WJ, Hou LX, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol 82:295–302

    CAS  Google Scholar 

  • Fu MM, Dawood M, Wang NH, Wu F (2019) Exogenous hydrogen sulfide reduces cadmium uptake and alleviates cadmium toxicity in barley. Plant Growth Regul 89(2):227–237

    CAS  Google Scholar 

  • Fuentes-Lara LO, Medrano-Macías J, Pérez-Labrada F, Rivas-Martínez EN, García-Enciso EL, González-Morales S, Juárez-Maldonado A, Rincón-Sánchez F, Benavides-Mendoza A (2019) From elemental sulfur to hydrogen sulfide in agricultural soils and plants. Molecules 24:2282

    CAS  PubMed Central  Google Scholar 

  • Garcia I, Gotor C, Romero LC (2015) Cysteine homeostasis. In: D’mello JPF (ed) Amino acids in higher plants. CABI Publishing, Wallingford, pp 219–233

    Google Scholar 

  • Ge Y, Hu KD, Wang SS, Hu LY, Chen XY, Li YH, Yang Y, Yang F, Zhang H (2017) Hydrogen sulfide alleviates postharvest ripening and senescence of banana by antagonizing the effect of ethylene. PLoS ONE 12:e0180113

    PubMed  PubMed Central  Google Scholar 

  • González-Morales S, Pérez-Labrada F, García-Enciso EL, Leija-Martínez P, Medrano-Macías J, Dávila-Rangel IE, Juárez-Maldonado A, Rivas-Martínez EN, Benavides-Mendoza A (2017) Selenium and sulfur to produce allium functional crops. Molecules 22(4):558

    PubMed Central  Google Scholar 

  • Goodwin MJ, Musa OM, Steed JW (2015) Problems associated with sour gas in the oilfield industry and their solutions. Energy Fuel 29(8):4667–4682

    CAS  Google Scholar 

  • Gotor C, Laureano-Marín AM, Moreno I, Aroca Á, García I, Romero LC (2015) Signaling in the plant cytosol: cysteine or sulfide? Amino Acids 47:2155–2164

    CAS  PubMed  Google Scholar 

  • Guo H, Xiao T, Zhou H, Xie Y, Shen W (2015) Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38:16

    Google Scholar 

  • Guo Z, Liang Y, Yan J, Yang E, Li K, Xu H (2018) Physiological response and transcription profiling analysis reveals the role of H2S in alleviating excess nitrate stress tolerance in tomato roots. Plant Physiol Biochem 124:59–69

    CAS  PubMed  Google Scholar 

  • Hancock JT, Whiteman M (2015) Hydrogen sulfide and reactive friends: the interplay with reactive oxygen species and nitric oxide signalling pathways. In: Hawkesford M, Rennenberg H, Saito K, Schnug E (eds) Molecular physiology and ecophysiology of sulfur. Springer, Cham, pp 153–168

    Google Scholar 

  • Hansen MH, Ingvorsen K, Jorgensen BB (1978) Mechanisms of hydrogen sulfide release from coastal marine sediments to the atmosphere. Limnol Oceanogr 23:68–76

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHMB, Mahmud JA, Nahar K, Mohsin SM, Parvin K, Fujita M (2018) Interaction of sulfur with phytohormones and signaling molecules in conferring abiotic stress tolerance to plants. Plant Signal Behav 13:1477905

    Google Scholar 

  • Hatzfeld Y, Maruyama A, Schmidt A, Noji M, Ishizawa K, Saito K (2000) β-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and arabidopsis. Plant Physiol 123:1163–1172

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 56:1481–1489

    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(4):396–406

    CAS  Google Scholar 

  • Hu LY, Hu SL, Wu J, Li YH, Zheng JL, Wei ZJ, Liu J, Wang HL, Liu YS, Zhang H (2012) Hydrogen sulfide prolongs postharvest shelf life of strawberry and plays an antioxidative role in fruits. J Agric Food Chem 60(35):8684–8693

    CAS  PubMed  Google Scholar 

  • Hussain S, Khalid MF, Saqib M, Ahmad S, Zafar W, Rao MJ, Morillon R, Anjum MA (2018) Drought tolerance in citrus rootstocks is associated with better antioxidant defense mechanism. Acta Physiol Plant 40(8):135

    Google Scholar 

  • Iqbal MJ (2018) Role of osmolytes and antioxidant enzymes for drought tolerance in wheat. Global Wheat Prod. https://doi.org/10.5772/intechopen.75926

    Article  Google Scholar 

  • 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 5:8251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Z, Pei Y (2016) Hydrogen sulfide: the shutter button of stomata in plants. Sci China Life Sci 59:1187–1188

    PubMed  Google Scholar 

  • Jin Z, Shen J, Qiao Z, Yang G, Wang R, Pei Y (2011) Hydrogen sulfide improves drought resistance in Arabidopsis thaliana. Biochem Biophys Res Comm 414(3):481–486

    CAS  PubMed  Google Scholar 

  • Jin Z, Xue S, Luo Y, Tian B, Fang H, Li H, Pei Y (2013) Hydrogen sulfide interacting with abscisic acid in stomatal regulation responses to drought stress in Arabidopsis. Plant Physiol Biochem 62:41–46

    CAS  PubMed  Google Scholar 

  • Johnson DW, Cole DW (1980) Anion mobility in soils: relevance to nutrient transport from forest ecosystems. Environ Int 3:79–90

    CAS  Google Scholar 

  • Joshi MM, Ibrahium IKA, Hollis JP (1975) Hydrogen sulphide: effects on the physiology of rice plants and relation to straighthead disease. Phytophatology 65:1165–1170

    CAS  Google Scholar 

  • Joshi NC, Yadav D, Ratner K, Kamara I, Aviv-Sharon E, Irihimovitch V, Charuvi D (2020) Sodium hydrosulfide priming improves the response of photosynthesis to overnight frost and day high light in avocado (Persea americana Mill, cv. ‘Hass’). Physiol Plant 168(2):394–405

    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

    CAS  PubMed  Google Scholar 

  • Kabil O, Banerjee R (2010) Redox biochemistry of hydrogen sulfide. J Biol Chem 285:21903–21907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kataoka T, Hayashi N, Yamaya T, Takahashi H (2004) Root-to-shoot transport of sulfate in arabidopsis. Evidence for the role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol 136:4198–4204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaya C, Ashraf M (2019) The mechanism of hydrogen sulfide mitigation of iron deficiency-induced chlorosis in strawberry (Fragaria × ananassa) plants. Protoplasma 256:371–382. https://doi.org/10.1007/s00709-018-1298-x

  • Khalid MF, Hussain S, Ahmad S, Ejaz S, Zakir I, Ali MA, Ahmed N, Anjum MA (2019) Impacts of abiotic stresses on growth and development of plant. Plant tolerance to environmental stress. CRC Press, Boca Raton, pp 1–8

    Google Scholar 

  • Khalid MF, Hussain S, Anjum MA, Ahmad S, Ali MA, Ejaz S, Morillon R (2020) Better salinity tolerance in tetraploid vs diploid volkamer lemon seedlings is associated with robust antioxidant and osmotic adjustment mechanisms. J Plant Physiol 244:153071

    CAS  PubMed  Google Scholar 

  • Kharbech O, Houmani H, Chaoui A, Corpas FJ (2017) Alleviation of Cr(VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPHrecycling metabolisms. J Plant Physiol 219:71–80

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kirschner S, Woodfield H, Prusko K, Koczor M, Gowik U, Hibberd JM, Westhoff P (2018) Expression of SULTR2;2, encoding a low-affinity sulphur transporter, in the Arabidopsis bundle sheath and vein cells is mediated by a positive regulator. J Exp Bot 69:4897–4906

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kourtidis K, Kelesis A, Petrakakis M (2008) Hydrogen sulfide (H2S) in urban ambient air. Atmos Environ 42(32):7476–7482

    CAS  Google Scholar 

  • Lai D, 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Léon S, Touraine B, Briat J-F, Lobréaux S (2002) The AtNFS2 gene from Arabidopsis thaliana encodes a NifS-like plastidial cysteine desulphurase. Biochem J 366:557–564

    PubMed  PubMed Central  Google Scholar 

  • Li ZG (2015) Analysis of some enzymes activities of hydrogen sulfide metabolism in plants. In: Cadenas E, Packer L (eds) Methods in enzymology. Academic Press, Cambridge, pp 253–269

    Google Scholar 

  • Li ZG, Gong M, Liu P (2012a) Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha Curcas”. Acta Physiol Plantarum 34(6):2207–2213

    CAS  Google Scholar 

  • Li ZG, Gong M, Xie H, Yang L, Li J (2012b) Hydrogen sulfide donor sodium hydrosulfide-induced heat tolerance in tobacco (Nicotiana tabacum L) suspension cultured cells and involvement of Ca2+ and calmodulin. Plant Sci 185:185–189

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Li SP, Hu KD, Hu LY, Li YH, Jiang AM, Xiao F, Han Y, Liu YS, Zhang H (2014) Hydrogen sulfide alleviates postharvest senescence of broccoli by modulating antioxidant defense and senescence-related gene expression. J Agric Food Chem 62(5):1119–1129

    CAS  PubMed  Google Scholar 

  • Li ZG, Xie LR, Li XJ (2015) Hydrogen sulfide acts as a downstream signal molecule in salicylic acid-induced heat tolerance in maize (Zea mays L.) seedlings. J Plant Physiol 177:121–127

    CAS  PubMed  Google Scholar 

  • Li Q, Wang Z, Zhao Y, Zhang X, Zhang S, Bo L, Wang Y, Ding Y, An L (2016a) Putrescine protect shul less barley from damage due to UV-B stress via H2S-and H2O2-mediated signaling pathways. Plant Cell Rep 35:1155–1168

    CAS  PubMed  Google Scholar 

  • Li ZG, Min X, Zhou ZH (2016b) Hydrogen sulfide: a signal molecule in plant cross-adaptation. Front Plant Sci 7:1621

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Liu R, Lal R (2015) Effects of low-level aqueous hydrogen sulfide and other sulfur species on lettuce (Lactuca sativa) seed germination. Commun Soil Sci Plant Anal 46:576–587

    CAS  Google Scholar 

  • Liu J, Hou L, Liu G, Liu X, Wang X (2011) Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. Chin Sci Bull 56(33):3547–3553

    CAS  Google Scholar 

  • Ma Q, Yang J (2018) Transcriptome profiling and identification of functional genes involved in H2S response in grapevine tissue cultured plantlets. Genes Genomics 40(12):1287–1300

    PubMed  Google Scholar 

  • Ma L, Yang L, Zhao J, Wei J, Kong X, Wang C, Zhang X, Yang Y, Hu X (2015) Comparative proteomic analysis reveals the role of hydrogen sulfide in the adaptation of the alpine plant Lamiophlomis rotate to altitude gradient in the Northern Tibetan Plateau. Planta 241:887–906

    CAS  PubMed  Google Scholar 

  • Ma D, Ding H, Wang C, Qin H, Han Q, Hou J, Lu H, Xie Y, Guo T (2016a) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS ONE 11(9):e0163082

    PubMed  PubMed Central  Google Scholar 

  • Ma D, Ding H, Wang C, Qin H, Han Q, Hou J et al (2016b) Alleviation of drought stress by hydrogen sulfide is partially related to the abscisic acid signaling pathway in wheat. PLoS ONE 2016(11):e0163082

    Google Scholar 

  • Ma X, Zheng G, Liang M, Xie D, Martinelli G, Sajjad W, Xu W, Fan Q, Li L, Du L, Zhao Y (2019) Occurrence and origin of H2S from volcanic reservoirs in Niudong area of the Santanghu Basin, NW China. Geofluids 2019:1279658

    Google Scholar 

  • Mostofa MG, Rahman A, Ansary MMU, Watanabe A, Fujita M, Tran LP (2015) Hydrogen sulfide modulates cadmium-induced physiological and biochemical responses to alleviate cadmium toxicity in rice. Sci Rep 5:14078

    PubMed  PubMed Central  Google Scholar 

  • Martin NM, Maricle BR (2015) Species-specific enzymatic tolerance of sulfide toxicity in plant roots. Plant Physiol Biochem 88:36–41

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maruyama-Nakashita A (2017) Metabolic changes sustain the plant life in low-sulfur environments. Curr Opin Plant Biol 39:144–151

    CAS  PubMed  Google Scholar 

  • Mathai JC, Missner A, Kügler P, Saparov SM, Zeidel ML, Lee JK, Pohl P (2009) No facilitator required for membrane transport of hydrogen sulfide. PNAS 106:16633–16638

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muñoz-Vargas MA, González-Gordo S, Cañas A, López-Jaramillo J, Palma JM, Corpas FJ (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 NO. Nitric Oxide 81:36–45

    PubMed  Google Scholar 

  • Nawaz F, Majeed S, Aqib M, Ahmad KS, Ghaffar A, Usmani MM, Shabbir RN, Shafiq BA (2020) Sulfur-mediated physiological and biochemical alterations to improve abiotic stress tolerance in food crops. In: Hasanuzzaman M (ed) Plant ecophysiology and adaptation under climate change: mechanisms and perspectives ii: mechanisms of adaptation and stress amelioration. Springer, Singapore, pp 415–441

    Google Scholar 

  • Mei YD, Chen HT, Shen WB, Shen W, Huang LQ (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:1–12

    Google Scholar 

  • Ni ZJ, Hu KD, Song CB, Ma RH, Li ZR, Zheng JL, Fu LH, Wei ZJ, Zhang H (2016) Hydrogen sulfide alleviates postharvest senescence of grape by modulating the antioxidant defenses. Oxid Med Cell Longev 2016:4715651

    PubMed  PubMed Central  Google Scholar 

  • Papanatsiou M, Scuffi D, Blatt MR, García-Mata C (2015) Hydrogen sulfide regulates inward-rectifying KC channels in conjunction with stomatal closure. Plant Physiol 168:29–35

    CAS  PubMed  PubMed Central  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007a) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants—from the field to the test tube and back. Plant Biol 9(5):582–588

    CAS  PubMed  Google Scholar 

  • Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt HN, Schmidt A (2007b) 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

    CAS  PubMed  Google Scholar 

  • Rennenberg H (1989) Synthesis and emission of hydrogen sulfide by higher plants. In: Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment. ACS Publications, Washington, DC, pp 44–57

    Google Scholar 

  • Riemenschneider A, Nikiforova V, Hoefgen R, De Kok LJ, Papenbrock J (2005) Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. Plant Physiol Biochem 43:473–483

    CAS  PubMed  Google Scholar 

  • Schröder P (1993) Plants as sources of atmospheric sulfur. In: Deok LJ, Stulen I, Rennenberg H, Brunold C, Rauser WE (eds) Sulfur nutrition and assimilation in higher plants: Regulatory, agricultural and environmental aspects. SPB Academic Publishing, The Hague, pp 253–270

    Google Scholar 

  • Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to L-Cysteine. Plant Physiol 70:430–436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen J, Xing T, Yuan H, Liu Z, Jin Z, Zhang L et al (2013) Hydrogen sulfide improves drought tolerance in Arabidopsis thaliana by microRNA expressions. PLoS ONE 8:e77047

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Ye T, Chan Z (2013) Exogenous application of hydrogen sulfide donor sodium hydrosulfide enhanced multiple abiotic stress tolerance in bermudagrass (Cynodon dactylon (L). Pers.). Plant Physiol Biochem 71:226–234

    CAS  PubMed  Google Scholar 

  • Shi H, Ye T, Han N, Bian H, Liu X, Chan Z (2015) Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis. J Integr Plant Biol 57:628–640

    CAS  PubMed  Google Scholar 

  • Shivaraj SM, Vats S, Bhat JA, Dhakte P, Goyal V, Khatri P, Kumawat S, Singh A, Prasad M, Sonah H, Sharma TR, Deshmukh R (2020) Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants. Physiol Plant 168:437–455

    CAS  PubMed  Google Scholar 

  • Singh SP, Schwan AL (2019) 4.18—sulfur metabolism in plants and related biotechnologies. In: Moo-Young M (ed) Comprehensive biotechnology, 3rd edn. Pergamon, Oxford, pp 221–236

    Google Scholar 

  • Singh S, Kumar V, Kapoor D, Kumar S, Singh S, Dhanjal DS, Datta S, Samuel J, Dey P, Wang S (2019) Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions. Physiol Plant 168:301

    PubMed  Google Scholar 

  • Spadaro D, Yun BW, Spoel SH, Chu C, Wang YQ, Loake GJ (2010) The redox switch: dynamic regulation of protein function by cysteine modifications. Physiol Plantarum 138:360–371

    CAS  Google Scholar 

  • Stuiver CEE, De Kok LJ, Kuiper PJC (1992) Freezing tolerance and biochemical changes in wheat shoots as affected by H2S fumigation. Plant Physiol Biochem 30:47–55

    CAS  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler RON, Miller GAD (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    CAS  PubMed  Google Scholar 

  • Tabatabai MA (2005) Sulfur in soils | overview. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 76–85

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tang X, An B, Cao D, Xu R, Wang S, Zhang Z, Liu X, Sun X (2020) Improving photosynthetic capacity, alleviating photosynthetic inhibition and oxidative stress under low temperature stress with exogenous hydrogen sulfide in blueberry seedlings. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00108

    Article  PubMed  PubMed Central  Google Scholar 

  • Tea I, Genter T, Naulet N, Boyer V, Lummerzheim M, Kleiber D (2004) Effect of foliar sulfur and nitrogen fertilization on wheat storage protein composition and dough mixing properties. Cereal Chem 81:759–766

    CAS  Google Scholar 

  • Thapa G, Sadhukhan A, Panda SK, Sahoo L (2012) Molecular mechanistic model of plant heavy metal tolerance. Biometals 25:489–505

    CAS  PubMed  Google Scholar 

  • Thompson CR, Kats G (1978a) Effects of continuous hydrogen sulphide fumigation on crop and forest plants. Environ Sci Technol 12:550–553

    CAS  Google Scholar 

  • Thompson CR, Kats G (1978b) Effects of continuous hydrogen sulfide fumigation on crop and forest plants. Environ Sci Technol 12(5):550–553

    CAS  Google Scholar 

  • Toohey JI (1989) Sulphane sulphur in biological systems: a possible regulatory role. Biochem J 264:625–632

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wainwright M (1984) Sulfur oxidation in soils. In: Brady NC (ed) Advances in agronomy. Academic Press, Cambridge, pp 349–396

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang R (2003) The gasotransmitter role of hydrogen sulfide. Antioxid Redox Sign. https://doi.org/10.1089/152308603768295249

    Article  Google Scholar 

  • Watts SF (2000) The mass budgets of carbonyl sulfide, dimethyl sulfide, carbon disulfide and hydrogen sulfide. Atmos Environ 34:761–779

    CAS  Google Scholar 

  • Wei GQ, Cao H, Sun YG, Deng B, Zhang WW, Yang HQ (2017) Effects of hydrogen sulfide on root architecture, leaf reactive oxygen and photosynthetic characteristics of Malus hupehensis under waterlogging. J Appl Ecol 28(10):3267–3273

    Google Scholar 

  • Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiol 61:184–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao M, Ma J, Li H, Jin H, Feng H (2010) Effects of hydrogen sulfide on alternative pathway respiration and induction of alternative oxidase gene expression in rice Suspension Cells. Zeitschrift für Naturforschung C 65:463–471

    CAS  Google Scholar 

  • Xiao Y, Wu X, Sun M, Peng F (2020) Hydrogen sulfide alleviates waterlogging-induced damage in peach seedlings via enhancing antioxidative system and inhibiting ethylene synthesis. Front Plant Sci 11:696

    PubMed  PubMed Central  Google Scholar 

  • 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 54:737–746

    CAS  PubMed  Google Scholar 

  • Xie Y, Zhang C, Lai D, 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(2):53–62

    CAS  PubMed  Google Scholar 

  • 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 41:465–476

    CAS  PubMed  Google Scholar 

  • Yao GF, Wei ZZ, Li TT, Tang J, Huang ZQ, Yang F, Li YH, Han Z, Hu F, Hu LY, Hu KD (2018) Modulation of enhanced antioxidant activity by hydrogen sulfide antagonization of ethylene in tomato fruit ripening. J Agric Food Chem 66(40):10380–10387

    CAS  PubMed  Google Scholar 

  • Yoshimoto N, Inoue E, Saito K, Yamaya T, Takahashi H (2003) Phloem-localizing sulfate transporter, Sultr1;3, mediates re-distribution of sulfur from source to sink organs in arabidopsis. Plant Physiol 131:1511–1517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Liao W (2020) Protein S-nitrosylation in plant abiotic stresses. Funct Plant Biol 47:1–10

    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

    CAS  PubMed  Google Scholar 

  • 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(12):1086–1094

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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(8):1031–1033

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Pei Y, Wang H, Jin Z, Liu Z, Qiao Z, Fang H, Zhang Y (2015) Hydrogen sulfide alleviates cadmium-induced cell death through restraining ROS accumulation in roots of Brassica rapa L. ssp. pekinensis. Oxid Med Cell Longev 2015:1–11

    Google Scholar 

  • Zhang P, Luo Q, Wang R, Xu J (2017) Hydrogen sulfide toxicity inhibits primary root growth through the ROS-NO pathway. Sci Rep 7:868

    PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Cai W, Ji TT, Ye L, Lu YT, Yuan TT (2020) WRKY13 enhances cadmium tolerance by promoting D-Cysteine Desulfhydrase and hydrogen sulfide production. Plant Physiol 183(1):345–357

    PubMed  PubMed Central  Google Scholar 

  • Zheng JL, Hu LY, Hu KD, Wu J, Yang F, Zhang H (2016) Hydrogen sulfide alleviates senescence of fresh-cut apple by regulating antioxidant defense system and senescence-related gene expression. Hort Sci 51:152–158

    CAS  Google Scholar 

  • Zhu CQ, Zhang JH, Sun LM, Zhu LF, Abliz B, Hu WJ, Zhong C, Bai ZG, Sajid H, Cao XC, Jin QY (2018) Hydrogen sulfide alleviates aluminum toxicity via decreasing apoplast and symplast alcontents in rice. Front Plant Sci 9:294

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agronomy, Pir Mehr Ali Shah, Arid Agriculture University, Rawalpindi, Pakistan

    Mukhtar Ahmed

  2. Department of Agricultural Research for Northern Sweden, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Mukhtar Ahmed

  3. Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, College of Tropical Crops, Hainan University, Haikou, 570228, Hainan, China

    Shah Fahad & Hongyan Liu

  4. Department of Agronomy, The University of Haripur, Haripur, Khyber Pakhtunkhwa, 22620, Pakistan

    Shah Fahad

  5. Department of Soil Science, Bahauddin Zakariya University, Multan, Pakistan

    Muhammad Arif Ali & Fariha Ilyas

  6. Department of Horticulture, Bahauddin Zakariya University, Multan, Pakistan

    Sajjad Hussain

  7. Department of Agronomy, Bahauddin Zakariya University, Multan, Pakistan

    Muhammad Tariq & Shakeel Ahmad

  8. Agronomy Section, Central Cotton Research Institute, Old Shuja Abad Road, Multan, Pakistan

    Muhammad Tariq

  9. Department of Horticultural, Northeast Agricultural University, Harbin, 150030, China

    Shah Saud

  10. Department of Environmental Sciences, Comsats University Islamabad, Islamabad, Pakistan

    Hafiz Mohkum Hammad

  11. Department of Agronomy, University College of Agriculture and Environmental Sciences, The Islamia University of Bahawalpur (IUB), Bahawalpur, Pakistan

    Wajid Nasim

  12. Guangxi Institute of Botany, Chinese Academy of Sciences, Guilin, China

    Chao Wu

Authors
  1. Mukhtar Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shah Fahad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Muhammad Arif Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sajjad Hussain
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Tariq
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fariha Ilyas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shakeel Ahmad
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shah Saud
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hafiz Mohkum Hammad
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wajid Nasim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hongyan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

For research articles with several authors, a short paragraph specifying their individual contributions must be provided. The following statements should be used: Conceptualization MA, SF, and SA; methodology MA, SH, MT, FI, and SU; software SA; validation HMH and WN; formal analysis CW; resources HL; writing—original draft preparation MA, SF, and SA; writing—review and editing, SF and MA; visualization SF, and supervision SF.

Corresponding author

Correspondence to Shah Fahad.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: Tariq Aftab.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmed, M., Fahad, S., Ali, M.A. et al. Hydrogen Sulfide: A Novel Gaseous Molecule for Plant Adaptation to Stress. J Plant Growth Regul 40, 2485–2501 (2021). https://doi.org/10.1007/s00344-020-10284-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10284-0

Keywords

Search

Navigation