Skip to main content

Advertisement

Log in

Hydrogen Sulfide: A new warrior in assisting seed germination during adverse environmental conditions

  • Review
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Seed, being a truly static period of the plant's existence, is exposed to a variety of biotic and abiotic shocks during dormancy that causes many cellular alterations. To improve its germination and vigor, the seed industry employs a variety of invigoration techniques, which are commonly referred to as seed priming procedures. The treatment with an exogenous H2S donor such as sodium hydrosulfide (NaHS) has been proven to improve seed germination. The H2S molecule is not only a key contributor to the signal transduction pathway meant for the sensation of seed exposure to various biotic and abiotic stresses but also contribute toward the alleviation of different abiotic stress. Although it was initially recognized as a toxic molecule, later its identification as a third gaseous transmitter molecule unveiled its potential role in seed germination, root development, and opening of stomata. Its involvement in cross talks with several other molecules, including plant hormones, also guides numerous physiological responses in the seeds, such as regulation of gene expression and enzymatic activities, which contribute to reliving various biological and non-biological stresses. However, the other metabolic pathways that could be implicated in the dynamics of the germination process when H2S is used are unclear. These pathways possibly may contribute to the seed germinability process with improved performance and stress tolerance. The present review briefly addresses the signaling and physiological impact of H2S in improving seed germination on exposure to various stresses.

Graphical abstract

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  • Ali B, Song WJ, Hu WZ et al (2014) Hydrogen sulfide alleviates lead-induced photosynthetic and ultrastructural changes in oilseed rape. Ecotoxicol Environ Saf 102:25–33

    Article  CAS  PubMed  Google Scholar 

  • Ali B, Qian P, Sun R et al (2015) Hydrogen sulfide alleviates the aluminum-induced changes in Brassica napus as revealed by physiochemical and ultrastructural study of plant. Environ Sci Pollut Res 22:3068–3081

    Article  CAS  Google Scholar 

  • Anamika MS, Singh B et al (2019) Databases: a weapon from the arsenal of bioinformatics for plant abiotic stress research. In: Wani SH (ed) Recent approaches in Omics for plant resilience to climate change. Springer, Cham, pp 135–169

    Chapter  Google Scholar 

  • Annadurai Y, Balasubramanian B, Arumugam VA et al (2022) Comprehensive strategies of Lignocellulolytic enzyme production from microbes and their applications in various commercial-scale faculties. Natr Resour Human Health 2(1):1–31

    Google Scholar 

  • Apel K, Hirt H (2004) REACTIVE OXYGEN SPECIES: Metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701

    Article  CAS  PubMed  Google Scholar 

  • Arif Y, Hayat S, Yusuf M, Bajguz A (2021) Hydrogen sulfide: a versatile gaseous molecule in plants. Plant Physiol Biochem 158:372–384

    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. https://doi.org/10.3389/fpls.2018.01369

    Article  PubMed  PubMed Central  Google Scholar 

  • Banerjee A, Roychoudhury A (2017) Abscisic-acid-dependent basic leucine zipper (bZIP) transcription factors in plant abiotic stress. Protoplasma 254:3–16

    Article  CAS  PubMed  Google Scholar 

  • Banerjee A, Tripathi DK, Roychoudhury A (2018) Hydrogen sulphide trapeze: environmental stress amelioration and phytohormone crosstalk. Plant Physiol Biochem 132:46–53

    Article  CAS  PubMed  Google Scholar 

  • Bao J, Ding TL, Jia WJ et al (2011) Effect of exogenous hydrogen sulfide on wheat seed germination under salt stress. Mod Agric Sci Technol 20:40–42

    Google Scholar 

  • Baudouin E, Poilevey A, Hewage NI et al (2016) The significance of hydrogen sulfide for Arabidopsis seed germination. Front Plant Sci 7:930

    Article  PubMed  PubMed Central  Google Scholar 

  • Bharti J, Mehta S, Ahmad S et al (2021) Mitogen-activated protein kinase, plants, and heat stress. In: Husen A (ed) Harsh environment and plant resilience. Springer, Cham, pp 323–354

    Chapter  Google Scholar 

  • Bharwana SA, Ali S, Farooq MA et al (2014) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res 21:717–731

    Article  CAS  Google Scholar 

  • Bloem E, Rubekin K, Haneklaus S et al (2011) H2S and COS gas exchange of transgenic potato lines with modified expression levels of enzymes involved in sulphur metabolism. J Agron Crop Sci 197:311–321

    Article  CAS  Google Scholar 

  • Cantliffe DJ, Fischer JM, Nell TA (1984) Mechanism of seed priming in circumventing thermodormancy in lettuce. Plant Physiol 75:290–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Wang W-H, Wu F-H et al (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:1–19

    Google Scholar 

  • Chen J, Shang Y-T, Wang W-H et al (2016) Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. Front Plant Sci 7:1173

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Andler SM, Goddard JM et al (2017) Integrating recognition elements with nanomaterials for bacteria sensing. Chem Soc Rev 46:1272–1283. https://doi.org/10.1039/C6CS00313C

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Yang B, Hao Z et al (2018) Exogenous hydrogen sulfide ameliorates seed germination and seedling growth of cauliflower under lead stress and its antioxidant role. J Plant Growth Regul 37:5–15

    Article  CAS  Google Scholar 

  • Chen Z, Huang Y, Yang W et al (2019) The hydrogen sulfide signal enhances seed germination tolerance to high temperatures by retaining nuclear COP1 for HY5 degradation. Plant Sci 285:34–43

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Jia H, Wang X 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 M, 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 

  • Choudhary KK, Chaudhary N (2021) Hydrogen sulfide and reactive oxygen species crosstalk and acquisition of abiotic stress tolerance. In: Singh S, Singh VP (eds) Hydrogen sulfide in plant biology. Elsevier, Amsterdam, pp 201–212

    Chapter  Google Scholar 

  • Choudhary JR, Get S, Tripathi A, Kaldate R, Rana M, Mehta S, Ahlawat J, Bansal M, Zaid A, Wani SH (2022) Breeding efforts for crop productivity in abiotic stress environment. In: Ansari SA, Ansari MI (eds) Augmenting crop productivity in stress environment. Springer, Singapore, pp 63–103

    Chapter  Google Scholar 

  • 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 64:1953–1966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas FJ (2019) Hydrogen sulfide: a new warrior against abiotic stress. Trends Plant Sci 24:983–988

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • da Silva CJ, Mollica DCF, Vicente MH, Peres LEP, Modolo LV (2018) NO, hydrogen sulfide does not come first during tomato response to high salinity. Nitric Oxide 76:164–173

    Article  Google Scholar 

  • Dai H, Jia G, Shan C (2015) Jasmonic acid-induced hydrogen peroxide activates MEK1/2 in upregulating the redox states of ascorbate and glutathione in wheat leaves. Acta Physiol Plant 37:1–6

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Deng Y-Q, Bao J, Yuan F et al (2016) Exogenous hydrogen sulfide alleviates salt stress in wheat seedlings by decreasing Na+ content. Plant Growth Regul 79:391–399

    Article  CAS  Google Scholar 

  • Ding H, Ma D, Huang X et al (2019) Exogenous hydrogen sulfide alleviates salt stress by improving antioxidant defenses and the salt overly sensitive pathway in wheat seedlings. Acta Physiol Plant 41:1–11

    Article  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 X, Jin Z, Liu D et al (2017) Hydrogen sulfide alleviates the cold stress through MPK4 in Arabidopsis thaliana. Plant Physiol Biochem 120:112–119

    Article  CAS  PubMed  Google Scholar 

  • Eun S, Shik Youn H, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365

    Article  CAS  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 

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

    Article  CAS  Google Scholar 

  • Filipovic MR, Jovanović 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 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  CAS  PubMed  Google Scholar 

  • Fu P, Wang W, Hou L, Liu X (2013) Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc Bot Pol. https://doi.org/10.5586/asbp.2013.031

    Article  Google Scholar 

  • Gao S-P, Hu K-D, Hu L-Y et al (2013) Hydrogen sulfide delays postharvest senescence and plays an antioxidative role in fresh-cut kiwifruit. HortScience 48:1385–1392

    Article  CAS  Google Scholar 

  • Golldack D, Lüking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    Article  CAS  PubMed  Google Scholar 

  • Gonai T, Kawahara S, Tougou M et al (2004) Abscisic acid in the thermoinhibition of lettuce seed germination and enhancement of its catabolism by gibberellin. J Exp Bot 55:111–118

    Article  CAS  PubMed  Google Scholar 

  • Guan MY, Zhang HH, Pan W et al (2018) Sulfide alleviates cadmium toxicity in Arabidopsis plants by altering the chemical form and the subcellular distribution of cadmium. Sci Total Environ 627:663–670

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Xiao T, Zhou H et al (2016) Hydrogen sulfide: a versatile regulator of environmental stress in plants. Acta Physiol Plant 38:16

    Article  Google Scholar 

  • Hao X, Jin Z, Wang Z et al (2020) Hydrogen sulfide mediates DNA methylation to enhance osmotic stress tolerance in Setaria italica L. Plant Soil 453:355–370

    Article  CAS  Google Scholar 

  • He H, Garcia-Mata C, He L-F (2019) Interaction between hydrogen sulfide and hormones in plant physiological responses. Plant Growth Regul 87:175–186

    Article  CAS  Google Scholar 

  • Horst WJ, Wang Y, Eticha D (2010) The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot 106:185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Z-Q, Ye S-C, Hu L-Y et al (2016) Hydrogen sulfide promotes wheat grain germination under cadmium stress. Proc Natl Acad Sci India Sect B Biol Sci 86:887–895

    Article  CAS  Google Scholar 

  • Huang D, Huo J, Liao W (2020) Hydrogen sulfide: roles in plant abiotic stress response and crosstalk with other signals. Plant Sci. https://doi.org/10.1016/j.plantsci.2020.110733

    Article  PubMed  Google Scholar 

  • Huo H, Dahal P, Kunusoth K et al (2013) Expression of 9-cis-EPOXYCAROTENOID DIOXYGENASE4 is essential for thermoinhibition of lettuce seed germination but not for seed development or stress tolerance. Plant Cell 25:884–900

    Article  CAS  PubMed  PubMed Central  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 5:1–13

    Article  CAS  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 

  • Jiang J, Chan A, Ali S et al (2016) Hydrogen sulfide—mechanisms of toxicity and development of an antidote. Sci Rep 6:1–10

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Joanna P, Barabasz-Krasny B, Lepiarczyk A et al (2019) Activity of the photosynthetic apparatus in Phaseolus vulgaris L. leaves under the cadmium stress. Not Bot Horti Agrobot Cluj-Napoca 47:405–411

    Google Scholar 

  • Katiyar RK, Sankhla MS, Mishra V et al (2022) Evaluation of toxicological metal profiling in different varieties of candies from the local market of Lucknow City. India Natr Resour Human Health 2(2):182–193

    Article  Google Scholar 

  • Kaya C, Aslan M (2020) Hydrogen sulphide partly involves in thiamine-induced tolerance to cadmium toxicity in strawberry (Fragaria x ananassa Duch) plants. Environ Sci Pollut Res 27:941–953

    Article  CAS  Google Scholar 

  • Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper (Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res 25:12612–12618

    Article  CAS  Google Scholar 

  • Kaya C, Akram NA, Ashraf M et al (2020a) Exogenously supplied silicon (Si) improves cadmium tolerance in pepper (Capsicum annuum L.) by up-regulating the synthesis of nitric oxide and hydrogen sulfide. J Biotechnol 316:35–45

    Article  CAS  PubMed  Google Scholar 

  • Kaya C, Sarıoğlu A, Ashraf M et al (2020b) Gibberellic acid-induced generation of hydrogen sulfide alleviates boron toxicity in tomato (Solanum lycopersicum L.) plants. Plant Physiol Biochem 153:53–63

    Article  CAS  PubMed  Google Scholar 

  • Khan MN, Mobin M, Abbas ZK, Siddiqui MH (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

    Article  PubMed Central  Google Scholar 

  • Khan MN, Siddiqui MH, Mukherjee S et al (2021) Calcium-hydrogen sulfide crosstalk during K+-deficient NaCl stress operates through regulation of Na+/H+ antiport and antioxidative defense system in mung bean roots. Plant Physiol Biochem 159:211–225

    Article  CAS  PubMed  Google Scholar 

  • Kharbech O, Ben MM, Sakouhi L et al (2020) Exogenous application of hydrogen sulfide reduces chromium toxicity in maize seedlings by suppressing NADPH oxidase activities and methylglyoxal accumulation. Plant Physiol Biochem 154:646–656

    Article  CAS  PubMed  Google Scholar 

  • Kokila R, Balasubramanian B, Meenambigai K et al (2021) A GIS-based tool for the analysis of the distribution and abundance of Chilo sacchariphagus indicus under the influence of biotic and abiotic factors. Environ Technol Innovation 21:101357

    Article  Google Scholar 

  • Kolupaev YE, Firsova EN, Yastreb TO et al (2019) Effect of hydrogen sulfide donor on antioxidant state of wheat plants and their resistance to soil drought. Russ J Plant Physiol 66:59–66

    Article  CAS  Google Scholar 

  • Kou N, Xiang Z, Cui W et al (2018) Hydrogen sulfide acts downstream of methane to induce cucumber adventitious root development. J Plant Physiol 228:113–120

    Article  CAS  PubMed  Google Scholar 

  • Kushwaha BK, Singh VP (2020) Mitigation of chromium (VI) toxicity by additional sulfur in some vegetable crops involves glutathione and hydrogen sulfide. Plant Physiol Biochem 155:952–964

    Article  CAS  PubMed  Google Scholar 

  • Lal SK, Kumar S, Sheri V et al (2018) Seed priming: an emerging technology to impart abiotic stress tolerance in crop plants. In: Rakshit A (ed) Advances in seed priming. Springer, Singapore, pp 41–50

    Google Scholar 

  • Li ZG (2013) Hydrogen sulfide: a multifunctional gaseous molecule in plants. Russ J Plant Physiol 60:733–740

    Article  CAS  Google Scholar 

  • Li ZG, He QQ (2015) Hydrogen peroxide might be a downstream signal molecule of hydrogen sulfide in seed germination of mung bean (Vigna radiata). Biologia (bratisl) 70:753–759

    Article  CAS  Google Scholar 

  • Li Z-G, Gong M, Liu P (2012a) Hydrogen sulfide is a mediator in H 2 O 2-induced seed germination in Jatropha Curcas. Acta Physiol Plant 34:2207–2213

    Article  CAS  Google Scholar 

  • Li ZG, Gong M, Xie H et al (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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Yi XY, Li YT (2014b) Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia (bratisl) 69:1001–1009

    Article  CAS  Google Scholar 

  • Li H, Gao MQ, Xue RL et al (2015a) Effect of hydrogen sulfide on D1 protein in wheat under drought stress. Acta Physiol Plant 37:1–9

    Article  Google Scholar 

  • Li ZG, Luo LJ, Sun YF (2015b) Signal crosstalk between nitric oxide and hydrogen sulfide may be involved in hydrogen peroxide-induced thermotolerance in maize seedlings. Russ J Plant Physiol 62:507–514

    Article  CAS  Google Scholar 

  • Li H, Li M, Wei X et al (2017) Transcriptome analysis of drought-responsive genes regulated by hydrogen sulfide in wheat (Triticum aestivum L.) leaves. Mol Genet Genomics 292:1091–1110

    Article  CAS  PubMed  Google Scholar 

  • Li ZG, Long WB, Yang SZ et al (2018) Signaling molecule methylglyoxal-induced thermotolerance is partly mediated by hydrogen sulfide in maize (Zea mays L.) seedlings. Acta Physiol Plant 40:1–10

    Article  Google Scholar 

  • Liu D, Li J, Li Z, Pei Y (2020a) Hydrogen sulfide inhibits ethylene-induced petiole abscission in tomato (Solanum lycopersicum L.). Hortic Res 7:1–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu F, Zhang X, Cai B et al (2020b) Physiological response and transcription profiling analysis reveal the role of glutathione in H2S-induced chilling stress tolerance of cucumber seedlings. Plant Sci 291:110363

    Article  CAS  PubMed  Google Scholar 

  • Luo S, Calderon-Urrea A, Jihua YU et al (2020) The role of hydrogen sulfide in plant alleviates heavy metal stress. Plant Soil 449:1–10

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Mehta S, James D, Reddy MK (2019) Omics technologies for abiotic stress tolerance in plants: current status and prospects. In: Wani SH (ed) Recent approaches in omics for plant resilience to climate change. Springer, Cham, pp 1–34

    Google Scholar 

  • Mehta S, Chakraborty A, Roy A et al (2021) Fight hard or die trying: current status of lipid signaling during plant–pathogen interaction. Plants 10:1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mei Y, Chen H, Shen W et al (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:1–12

    Article  Google Scholar 

  • Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler RON (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mishra V, Singh VP (2021) Implication of nitric oxide and hydrogen sulfide signalling in alleviating arsenate stress in rice seedlings. Environ Pollut 291:117958

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Nonogaki H, Bassel GW, Bewley JD (2010) Germination—still a mystery. Plant Sci 179:574–581. https://doi.org/10.1016/j.plantsci.2010.02.010

    Article  CAS  Google Scholar 

  • Nyarukowa C, Koech R, Kamunya S et al (2021) UPLC-MS based metabolomics analysis reveals metabolite compositional differences between Kenyan commercial and non commercial black tea (Camellia sinensis L.) cultivars. Natr Resour Human Health 1(1):19–29

    Article  Google Scholar 

  • Pan D-Y, Fu X, Zhang X-W et al (2020) Hydrogen sulfide is required for salicylic acid–induced chilling tolerance of cucumber seedlings. Protoplasma 257:1543–1557

    Article  CAS  PubMed  Google Scholar 

  • Pandey V, Pati AK (2016) A new candidate of catalase appears during the germination after priming in naturally aged neem (Azadirachta indica) seeds. J Plant Biochem Physiol 4:1–4. https://doi.org/10.4172/2329-9029.1000171

    Article  CAS  Google Scholar 

  • Pandey V, Pati AK (2017) Limitation of improvement in germination by osmopriming of differentially aged non-orthodox neem (Azadirachta indica) seedstle. Biochem Physiol Open Access 6:1–7. https://doi.org/10.4172/2168-9652.1000217

    Article  CAS  Google Scholar 

  • Pandey P, Pallujam AD, Leelavathi S et al (2021) Nitric oxide: a key modulator of plant responses under environmental stress. In: Husen A (ed) Plant performance under environmental stress. Springer, Cham, pp 301–328

    Chapter  Google Scholar 

  • Parmar H, Venkatapuram AK, Rashid A et al (2022) Portfolio of drought stress response and genetic enhancement strategies for development of future drought-tolerant crop. In: Vaishnav A, Arya SS (eds) Plant stress mitigators. Springer, Singapore, pp 515–539

    Chapter  Google Scholar 

  • Paul K, Daniel T, Adamou Ibrahima A (2022) Factors affecting vegetation dynamics in the south of the Mokolo District in the Far North of Cameroon. Natr Resour Human Health 2(2):208–214

    Article  Google Scholar 

  • Qi Q, Guo Z, Liang Y et al (2019) Hydrogen sulfide alleviates oxidative damage under excess nitrate stress through MAPK/NO signaling in cucumber. Plant Physiol Biochem 135:1–8

    Article  CAS  PubMed  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 

  • Rajjou L, Duval M, Gallardo K et al (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533

    Article  CAS  PubMed  Google Scholar 

  • Rezania S, Kamyab H, Rupani PF et al (2021) Recent advances on the removal of phosphorus in aquatic plant-based systems. Environ Technol Innovation 24:101933

    Article  CAS  Google Scholar 

  • Rizwan M, Mostofa MG, Ahmad MZ et al (2019) Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel. Plant Physiol Biochem 138:100–111

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury A, Ghosh S, Paul S et al (2016) Pre-treatment of seeds with salicylic acid attenuates cadmium chloride-induced oxidative damages in the seedlings of mungbean (Vigna radiata L. Wilczek). Acta Physiol Plant 38:11

    Article  Google Scholar 

  • Sahil KR, Das A, Mehta S et al (2021a) Jasmonic acid for sustainable plant growth and production under adverse environmental conditions. In: Husen A (ed) Plant performance under environmental stress. Springer, Cham, pp 71–98

    Chapter  Google Scholar 

  • Sahil KR, Mehta S et al (2021b) Salicylic acid for vigorous plant growth and enhanced yield under harsh environment. In: Husen A (ed) Plant performance under environmental stress. Springer, Cham, pp 99–127

    Chapter  Google Scholar 

  • Sahil KR, Patra A et al (2021c) Expression and regulation of stress-responsive genes in plants under harsh environmental conditions. In: Husen A (ed) Harsh environment and plant resilience. Springer, Cham, pp 25–44

    Chapter  Google Scholar 

  • Samma MK, Zhou H, Cui W et al (2017) Methane alleviates copper-induced seed germination inhibition and oxidative stress in Medicago sativa. Biometals 30:97–111

    Article  CAS  PubMed  Google Scholar 

  • Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci 239:44–55

    Article  CAS  PubMed  Google Scholar 

  • Scuffi D, Lamattina L, García-Mata C (2016) Gasotransmitters and stomatal closure: Is there redundancy, concerted action, or both? Front Plant Sci 7:277

    Article  PubMed  PubMed Central  Google Scholar 

  • Shan C, Dai H, Sun Y (2012) Hydrogen sulfide protects wheat seedlings against copper stress by regulating the ascorbate and glutathione metabolism in leaves. Aust J Crop Sci 6:248–254

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Shan C, Zhang S, Zhou Y (2017) Hydrogen sulfide is involved in the regulation of ascorbate-glutathione cycle by exogenous ABA in wheat seedling leaves under osmotic stress. Cereal Res Commun 45:411–420

    Article  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Sharma P, Sharma MM, Patra A, Vashisth M, Mehta S, Singh B, Tiwari M, Pandey V (2020a) The role of key transcription factors for cold tolerance in plants. In: Wani SH (ed) Transcription factors for abiotic stress tolerance in plants. Academic Press, Cambridge, pp 123–152

    Chapter  Google Scholar 

  • Sharma P, Sharma MM, Kapoor D, Rani K, Singh D, Barkodia M (2020b) Role of microbes for attaining enhanced food crop production. In: Singh J, Vyas A (eds) Microbial biotechnology: basic research and applications. Springer, Cham, pp 55–78

    Chapter  Google Scholar 

  • Sharma MM, Sharma P, Kapoor D, Beniwal P, Mehta S (2021a) Phytomicrobiome community: an agrarian perspective towards resilient agriculture. In: Husen A (ed) Plant performance under environmental stress. Springer, Cham, pp 493–534

    Chapter  Google Scholar 

  • Sharma P, Pandey V, Sharma MM, Patra A, Singh B, Mehta S, Husen A (2021b) A Review on biosensors and nanosensors application in agroecosystems. Nanoscale Res Lett 16(1):1–24

    Article  Google Scholar 

  • Sharma P, Sangwan S, Kumari A, Singh S, Kaur H (2022) Impact of climate change on soil microorganisms regulating nutrient transformation. In: Vaishnav A, Arya SS (eds) Plant stress mitigators. Springer, Singapore, pp 145–172

    Chapter  Google Scholar 

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

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Singh VP, Tripathi DK, Fotopoulos V (2020) Hydrogen sulfide and nitric oxide signal integration and plant development under stressed/non-stressed condition. Physiol Plant. https://doi.org/10.1111/ppl.13066

    Article  PubMed  Google Scholar 

  • Singh A, Mehta S, Yadav S et al (2022) How to Cope with the challenges of environmental stresses in the era of global climate change: an update on ROS stave off in plants. Int J Mol Sci 23:1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun YD, Luo WR (2014) Effects of exogenous hydrogen sulphide on seed germination and seedling growth of cucumber (Cucumis sativus) under sodium bicarbonate stress. Seed Sci Technol 42:126–131

    Article  Google Scholar 

  • Szőllősi R, Hodács VK (2022) Physiological roles of hydrogen sulfide under heavy metal stress. In: Tariq M, Aftab T (eds) Emerging plant growth regulators in agriculture. Elsevier, Amsterdam, pp 317–334

    Chapter  Google Scholar 

  • Tang X, An B, Cao D et al (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 

  • Tian B, Zhang Y, Jin Z et al (2017) Role of hydrogen sulfide in the methyl jasmonate response to cadmium stress in foxtail millet. Front Biosci 22:530–538

    Article  CAS  Google Scholar 

  • Toh S, Imamura A, Watanabe A et al (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyagi A, Sharma S, Ali S, Gaikwad K (2021) Crosstalk between H2S and NO: an emerging signalling pathway during waterlogging stress in legume crops. Plant Biol. https://doi.org/10.1111/plb.13319

    Article  PubMed  Google Scholar 

  • Valivand M, Amooaghaie R, Ahadi A (2019) Seed priming with H2S and Ca2+ trigger signal memory that induces cross-adaptation against nickel stress in zucchini seedlings. Plant Physiol Biochem 143:286–298

    Article  CAS  PubMed  Google Scholar 

  • Vibhuti Bargali K, Bargali SS (2022) Changing pattern of plant species utilization in relation to altitude and their relative prevalence in homegardens of Kumaun Himalaya. India Natr Resour Human Health 2(2):253–264

    Article  Google Scholar 

  • Viswanath KK, Varakumar P, Pamuru RR et al (2020) Plant lipoxygenases and their role in plant physiology. J Plant Biol 63:83–95

    Article  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 H-R, Che Y-H, Huang D, Ao H (2020) Hydrogen sulfide mediated alleviation of cadmium toxicity in Phlox paniculata L. and establishment of a comprehensive evaluation model for corresponding strategy. Int J Phytoremediation 22:1085–1095

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Deng Y, Liu Z, Liao W (2021) Hydrogen sulfide in plants: crosstalk with other signal molecules in response to abiotic stresses. Int J Mol Sci 22:12068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309

    Article  CAS  PubMed  Google Scholar 

  • Wu GX, Cai BB, Zhou CF et al (2016) Hydrogen sulfide-induced chilling tolerance of cucumber and involvement of nitric oxide. J Plant Biol Res 5:58–69

    Google Scholar 

  • Wu GX, Li DD, Sun C et al (2017) Hydrogen sulfide interacts with Ca2+ to enhance chilling tolerance of cucumber seedlings. Chin J Biochem Mol Biol 33:1037–1046

    CAS  Google Scholar 

  • Yadav B, Jogawat A, Lal SK et al (2021) Plant mineral transport systems and the potential for crop improvement. Planta 253:1–30

    Google Scholar 

  • Yamasaki H, Cohen MF (2016) Biological consilience of hydrogen sulfide and nitric oxide in plants: gases of primordial earth linking plant, microbial and animal physiologies. Nitric Oxide 55:91–100

    Article  PubMed  Google Scholar 

  • Ye S-C, Hu L-Y, Hu K-D et al (2015) Hydrogen sulfide stimulates wheat grain germination and counteracts the effect of oxidative damage caused by salinity stress. Cereal Res Commun 43:213–224

    Article  CAS  Google Scholar 

  • Ye X-Y, Qiu X-M, Sun Y-Y, Li Z-G (2020) Interplay between hydrogen sulfide and methylglyoxal initiates thermotolerance in maize seedlings by modulating reactive oxidative species and osmolyte metabolism. Protoplasma 257:1415–1432

    Article  PubMed  Google Scholar 

  • Yu L, Zhang C, Shang H et al (2013) Exogenous hydrogen sulfide enhanced antioxidant capacity, amylase activities and salt tolerance of cucumber hypocotyls and radicles. J Integr Agric 12:445–456

    Article  Google Scholar 

  • Zanganeh R, Jamei R, Rahmani F (2019) Role of salicylic acid and hydrogen sulfide in promoting lead stress tolerance and regulating free amino acid composition in Zea mays L. Acta Physiol Plant 41:1–9

    Article  CAS  Google Scholar 

  • Zanganeh R, Jamei R, Rahmani F (2020) Pre-sowing seed treatment with salicylic acid and sodium hydrosulfide confers Pb toxicity tolerance in maize (Zea mays L.). Ecotoxicol Environ Saf 206:111392

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hu L, Hu K et al (2008) Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J Integr Plant Biol 50:1518–1529

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Tang J, Liu X et al (2009) Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J Integr Plant Biol 51:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Dou W, Jiang C-X et al (2010a) Hydrogen sulfide stimulates β-amylase activity during early stages of wheat grain germination. Plant Signal Behav 5:1031–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Hu L-Y, Li P et al (2010b) Hydrogen sulfide alleviated chromium toxicity in wheat. Biol Plant 54:743–747

    Article  CAS  Google Scholar 

  • Zhang H, Jiao H, Jiang C-X et al (2010c) Hydrogen sulfide protects soybean seedlings against drought-induced oxidative stress. Acta Physiol Plant 32:849–857

    Article  CAS  Google Scholar 

  • Zhang H, Wang MJ, Hu LY et al (2010d) Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ J Plant Physiol 57:532–539

    Article  CAS  Google Scholar 

  • Zhang X-W, Liu F-J, Zhai J et al (2020) Auxin acts as a downstream signaling molecule involved in hydrogen sulfide-induced chilling tolerance in cucumber. Planta 251:1–19

    Article  Google Scholar 

  • Zhao M, Liu Q, Zhang Y et al (2020) Alleviation of osmotic stress by H2S is related to regulated PLDα1 and suppressed ROS in Arabidopsis thaliana. J Plant Res. https://doi.org/10.1007/s10265-020-01182-3

    Article  PubMed  Google Scholar 

  • 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 9:1288

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou H, Chen Y, Zhai F et al (2020) Hydrogen sulfide promotes rice drought tolerance via reestablishing redox homeostasis and activation of ABA biosynthesis and signaling. Plant Physiol Biochem 155:213–220

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The authors are grateful to the MJIIT-KL Universiti Teknologi Malaysia. The financial support from the EU supported project Sustainable Process Integration Laboratory–SPIL funded as project No. CZ.02.1.01/0.0/0.0/15_003/0000456, by Czech Republic Operational Programme Research and Development, Education, Priority 1: Strengthening capacity for quality research under the collaboration agreement with Universiti Teknologi Malaysia, Johor Bahru has also been gratefully acknowledged. Mohsen Mesbah is a researcher of UTM under the Post-Doctoral Fellowship Scheme with Vote Number R.K130000.7113.05E83.

Author information

Authors and Affiliations

Authors

Contributions

This review article was carried out in collaboration with the authors. Writing-original draft, PS, AM: Draft preparation, review, and editing, selected bibliographic sources, ME, MMMS, SM, VP, WL, RB, MM, SC, and BB: Conceptualization, Writing-review and editing, proofreading, supervising.; HK., JJK., BB: Coordinated the working group, AM, ME, BB. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Hesam Kamyab, Balamuralikrishnan Balasubramanian or Mohsen Mesbah.

Ethics declarations

Conflict of interest

The authors declare that there are no conflict of interest.

Ethical approval and consent to participate

Not applicable.

Consent to publish

Not applicable.

Additional information

Communicated by Carlos Garcia-Mata

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, P., Meyyazhagan, A., Easwaran, M. et al. Hydrogen Sulfide: A new warrior in assisting seed germination during adverse environmental conditions. Plant Growth Regul 98, 401–420 (2022). https://doi.org/10.1007/s10725-022-00887-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-022-00887-w

Keywords

Navigation