Skip to main content

Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings

Abstract

Hydrogen sulfide (H2S) is a signal molecule that is involved in plant growth, development and the acquisition of stress tolerance including heat tolerance, but the mechanism of H2S-induced heat tolerance is not completely clear. In present study, the effect of sodium hydrosulfide (NaHS), a H2S donor, treatment on heat tolerance of maize seedlings in relation to antioxidant system was investigated. The results showed that NaHS treatment improved survival percentage of maize seedlings under heat stress in a concentration-dependent manner, indicating that H2S treatment could improve heat tolerance of maize seedlings. To further study mechanism of NaHS-induced heat tolerance, catalase (CAT), guaiacol peroxidase (GPX), superoxide dismutase (SOD), glutathione reductase (GR) and ascorbate peroxidase (APX) activities, and glutathione (GSH) and ascorbic acid (AsA) contents in maize seedlings were determined. The results showed that NaHS treatment increased the activities of CAT, GPX, SOD and GR, and GSH and AsA contents as well as the ratio of reduced antioxidants to total antioxidants [AsA/(AsA+DHA) and GSH/(GSH +GSSG)] in maize seedlings under normal culture conditions compared with the control. Under heat stress, antioxidant enzymes activities, antioxidants contents and the ratio of the reduced antioxidants to total antioxidants in control and treated seedlings all decreased, but NaHS-treated seedlings maintained higher antioxidant enzymes activities and antioxidants levels as well as the ratio of reduced antioxidants to total antioxidants. All of above-mentioned results suggested that NaHS treatment could improve heat tolerance of maize seedlings, and the acquisition of this heat tolerance may be relation to enhanced antioxidant system activity.

This is a preview of subscription content, access via your institution.

Abbreviations

ANOVA:

analysis of variance

APX:

ascorbate peroxidase

AsA:

ascorbic acid

CAT:

catalase

CO:

carbon monoxide

DTT:

dithiothreitol

DHA:

dehydroascorbate

FW:

fresh weight

GR:

glutathione reductase

GSH:

glutathione

GSSG:

oxidized glutathione

GST:

glutathione S-transferase

MDA:

malondialdehyde

NO:

nitric oxide

NBT:

nitroblue tetrazolium

GPX:

guaiacol peroxidase

ROS:

reactive oxygen species

SOD:

superoxide dismutase

TBA:

2-thiobarbituric acid

TCA:

trichloroacetic acid

References

  • Ahmad P., Jaleel C.A., Salem M.A., Nabi G. & Sharma S. 2010. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit. Rev. Biotechnol. 30: 161–175.

    CAS  PubMed  Article  Google Scholar 

  • Bloem E., Rubekin K., Haneklaus S., Banfalvi Z., Hesse H. & Schnug E. 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.

    CAS  Article  Google Scholar 

  • Chen J., Wang W.H., Wu F.H., You C.Y., Liu W.T., Dong X.K., He J.X. & Zheng H.L. 2013. Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. Plant Soil 362: 301–318.

    CAS  Article  Google Scholar 

  • Christou A., Manganaris G.A., 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.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Christou A., Filippou P., Manganaris G.A. & 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 Central  PubMed  Article  Google Scholar 

  • Foyer C.H. & Noctor G. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid. Red. Signal. 11: 861–905.

    CAS  Article  Google Scholar 

  • Foyer C.H. & Noctor G. 2011. Ascorbate and glutathione: The heart of the redox hub. Plant Physiol. 155: 2–18.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Fu P.N., Wang W.J., Hou L.X. & Liu X. 2013. Hydrogen sulfide is involved in the chilling stress response in Vitis vinifera L. Acta Soc. Bot. Pol. 82: 295–302.

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  • Garg N. & Kaur H. 2013. Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) millsp. genotypes colonized by arbuscular mycorrhizal fungi. J. Agron. Crop. Sci. 199: 118–133.

    CAS  Article  Google Scholar 

  • Grover A., Mittal D., Negi M. & Lavania D. 2013. Generating high temperature tolerant transgenic plants: Achievements and challenges. Plant Sci. 205/206: 38–47.

    Article  Google Scholar 

  • Hancock J.T., Lisjak M., Teklic T., Wilson I.D. & Whiteman M. 2011. Hydrogen sulphide and signalling in plants. CAB Rev.: Perspect. Agric. Vet. Sci. Nutr. Nat. Resour. 6: 1–7.

    Article  Google Scholar 

  • Hancock J.T. & Whiteman M. 2014. Hydrogen sulfide and cell signaling: Team player or referee? Plant Physiol. and Biochem. 78: 37–42.

    CAS  Google Scholar 

  • Jaleel C.A., Riadhm K., Gopi R., Manivannan P., Ines J., Al-Juburi H.J., Zhao C.X., Shao H.B. & Panneerselvam R. 2009. Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plant. 31: 427–436.

    Google Scholar 

  • Jin Z.P., Xue S.W., Luo Y.N., Fang B.H., Tian H.H., Li H. & Pei Y.X. 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 

  • Leipner J. & Stamp P. 2009. Chilling stress in maize seedlings, pp. 291–344. In: Bennetzen J.L. & Hake S.C. (eds), Handbook of maize: Its biology. Springer, New York.

    Chapter  Google Scholar 

  • Li L., Rose P. & Moore P.K. 2011 Hydrogen sulfide and cell signaling. Annu. Rev. Pharmacol. Toxicol. 51: 169–187.

    CAS  PubMed  Article  Google Scholar 

  • Li Z.G. 2013. Hydrogen sulfide: a multifunctional gaseous molecule in plants. Russ. J. Plant Physiol. 6: 733–740.

    Google Scholar 

  • Li Z.G., Ding X.J. & Du P.F. 2013a. Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. J. Plant Physiol. 170: 741–747.

    CAS  PubMed  Article  Google Scholar 

  • Li Z.G. & Gong M. 2011. Mechanical stimulation-induced crossadaptation in plants: An overview. J. Plant Biol. 54: 358–364.

    Article  Google Scholar 

  • Li Z.G., Gong M. & Liu P. 2012a. Hydrogen sulfide is a mediator in H2O2-induced seed germination in Jatropha curcas. Acta Physiol Plant 34: 2207–2213

    CAS  Google Scholar 

  • Li Z.G., 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. 185/186: 185–189.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Li Z.G., Yang S.Z., Long W.B., Yang G.X. & Shen Z.Z. 2013b. Hydrogen sulfide may be a novel downstream signal molecule in nitric oxide-induced heat tolerance of maize (Zea mays L.) seedlings. Plant Cell Environ. 36: 1564–1572.

    CAS  PubMed  Article  Google Scholar 

  • Li Z.G., Yuan L.X., Wang Q.L., Ding Z.L. & Dong C.Y. 2013b. Combined action of antioxidant defense system and osmolytes in chilling shock-induced chilling tolerance in Jatropha curcas seedlings. Acta Physiol. Plant. 35: 2127–2136.

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lisjak M., Teklic T., Wilson I.D., Whiteman M., Hancock J.T. 2013 Hydrogen sulfide: Environmental factor or signalling molecule? Plant Cell Environ. 36: 1607–1616.

    CAS  PubMed  Article  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: 3547–3553.

    CAS  Article  Google Scholar 

  • Mittler R., Finka A., Goloubinoff P. 2012. How do plants feel the heat? Trends Biochem. Sci. 37: 118–125.

    CAS  PubMed  Article  Google Scholar 

  • Piterková J., Luhová L., Mieslerová B., Lebeda A. & Petřivalský M. 2013. Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Sci. 207: 57–65.

    PubMed  Article  Google Scholar 

  • Saidi Y., Finka A. & Goloubinoff P. 2011. Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol. 190: 556–565.

    CAS  PubMed  Article  Google Scholar 

  • Scheibe R. & Dietz K.J. 2012. Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ. 35: 202–216.

    CAS  PubMed  Article  Google Scholar 

  • Shan C.J., Zhang S.L., Li D.F., Zhao Y.Z., Tian X.L., Zhao X.L., Wu Y.X., Wei X.Y. & Liu R.Q. 2011 Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. Acta Physiol. Plant. 33: 2533–2540.

    CAS  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 

  • Strable J. & Scanlon M.J. 2009. Maize (Zea mays): A model organism for basic and applied research in plant biology. Cold spring harbor protocols 2009(10):pdb.emo132

    Google Scholar 

  • Szarka A., Tomasskovics B. & Bánhegyi G. 2012. The ascorbateglutathione-α-tocopherol triad in abiotic stress response. Inter. J. Mol. Sci. 13: 4458–4483.

    CAS  Article  Google Scholar 

  • Tari I., Laskay G., Takács Z. & Poór P. 2013. Response of sorghum to abiotic stresses: A Review. J. Agron. Crop. Sci. 199: 264–274.

    CAS  Article  Google Scholar 

  • Wahid A., Gelani S., Ashraf M. & Foolad M.R. 2007. Heat tolerance in plants: An overview. Environ Exp Bot 61: 199–223.

    Article  Google Scholar 

  • Wang R. 2012. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol. Rev. 92: 791–896.

    CAS  PubMed  Article  Google Scholar 

  • Wang B.L., Shi L., Li Y.X. & Zhang W.H. 2010. Boron toxicity is alleviated by hydrogen sulWde in cucumber (Cucumis sativus L.) seedlings. Planta 231: 1301–1309.

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  • Wu D.H., Li Y.L., Xia X., Pu Z.P., Liao J.M., Huang K. & Li Z.G. 2013. Hydrogen sulfide donor sodium hydrosulfide pretreatment improved multiple resistance abilities of wheat to high temperature and drought stress. J. Yunnan. Norm. Univ. Nat. Sci. 33: 29–35.

    Google Scholar 

  • Wu H.C., Luo D.L., Vignols F. & Jinn T.L. 2012. Heat shockinduced biphasic Ca2+ signature and OsCaM1-1 nuclear localization mediate downstream signalling in acquisition of thermotolerance in rice (Oryza sativa L.). Plant Cell Environ. 35: 1543–1557.

    CAS  PubMed  Article  Google Scholar 

  • Zhang H., Hu L.Y., Hu K.D., He Y.D., Wang S.H. & Luo J.P. 2008 Hydrogen sulfide promotes wheat seed germination and alleviates oxidative damage against copper stress. J. Integr. Plant Biol. 50: 1518–1529.

    CAS  PubMed  Article  Google Scholar 

  • Zhang H., Hu LY., Li P., Hu K.D., Jiang C.X. & Luo J.P. 2010a. Hydrogen sulfide alleviated chromium toxicity in wheat. Biol. Plant. 54: 743–747.

    CAS  Article  Google Scholar 

  • Zhang H., Hua S.L., Zhang Z.J., Hua L.Y., Jiang C.X., Wei Z.J., Liu J., Wang H.L. & Jiang S.T. 2011 Hydrogen sulfide acts as a regulator of flower senescence in plants. Postharv. Biol. Technol. 60: 251–257.

    CAS  Article  Google Scholar 

  • Zhang H., Tang J., Liu X.P., Wang Y., Yu W., Peng W.P., Fang F., Ma D.F., Wei Z.J. & Hu L.Y. 2009a. Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. J. Integr. Plant Biol. 51: 1084–1092.

    Google Scholar 

  • Zhang H., Wang M.F., Hua L.Y., Wang S.H., Hua K.D., Bao L.J. & Luo J.P. 2010b. Hydrogen sulfide promotes wheat seed germination under osmotic stress. Russ. J. Plant Physiol. 57: 532–539.

    CAS  Google Scholar 

  • Zhang H., Ye Y.K., Wang S.H., Luo J.P., Tang J. & Ma D.F. 2009b. Hydrogen sulfide counteracts chlorophyll loss in sweet potato seedling leaves and alleviates oxidative damage against osmotic stress. Plant Growth Regul. 58: 243–250.

    CAS  Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhong-Guang Li.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, ZG., Yi, XY. & Li, YT. Effect of pretreatment with hydrogen sulfide donor sodium hydrosulfide on heat tolerance in relation to antioxidant system in maize (Zea mays) seedlings. Biologia 69, 1001–1009 (2014). https://doi.org/10.2478/s11756-014-0396-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11756-014-0396-2

Key words

  • antioxidants
  • antioxidant enzymes
  • heat stress
  • heat tolerance
  • hydrogen sulfide
  • maize seedlings