Hydrogen Peroxide is Involved in the Regulation of Ascorbate and Glutathione Metabolism in Wheat Leaves under Water Stress

Abstract

This study investigated the regulation of ascorbic acid and glutathione metabolism by hydrogen peroxide in wheat leaves under water stress. The results showed that H2O2 level, the activities of ascorbate peroxidase, glutathione reductase, monodehydroascorbate reductase, dehydroascorbate reductase, L-galactono-1,4-lactone dehydrogenase and gamma-glutamylcysteine synthetase, and the contents of reduced ascorbate, reduced glutathione, total ascorbate and total glutathione were increased by water stress. And above increases were suppressed by pre-treatment with NADPH oxidase inhibitor diphenyleneiodonium chloride. Application of DPI also reduced H2O2 level, the activities of γ-ECS, GalLDH, APX, GR, DHAR and MDHAR, and the contents of AsA, GSH, total ascorbate and total glutathione, compared with control. Application of H2O2 to DPI-inhibited wheat seedlings prevented the reduction in the activities of APX, GR, MDHAR, DHAR, GalLDH and γ-ECS, and the contents of AsA, GSH, total ascorbate and total glutathione induced by DPI under water stress. Meanwhile, pre-treatment with DPI increased the malondialdehyde content and electrolyte leakage. Application of H2O2 to DPI-inhibited wheat seedlings prevented the increases in MDA content and EL. Our results suggested that water stress-induced H2O2 is a signal that leads to the up-regulation of ascorbate and glutathione metabolism and has an important role for acquisition of water-stress tolerance in wheat.

Abbreviations

APX:

ascorbate peroxidase

DHAR:

dehydroascorbate reductase

DPI:

diphenyleneiodonium chloride

EL:

electrolyte leakage

γ-ECS:

gamma-glutamylcysteine synthetase

GR:

glutathione reductase

H2O2:

hydrogen peroxide

GalLDH:

L-galactono-1,4-lactone dehydrogenase

MDA:

malondialdehyde

MDHAR:

monodehydroascorbate reductase

AsA:

reduced ascorbate

GSH:

reduced glutathione

References

  1. Alavi-Samani, S.M., Kachouei, M.A., Pirbalouti, A.G. 2015. Growth, yield, chemical composition, and antioxidant activity of essential oils from two thyme species under foliar application of jasmonic acid and water deficit conditions. Hortic. Environ. Biotechnol. 56:411–420.

    CAS  Article  Google Scholar 

  2. Andriunas, F.A., Zhang, H.M., Xia, X., Offler, C.E., McCurdy, D.W., Patrick, J.W. 2012. Reactive oxygen species form part of a regulatory pathway initiating trans-differentiation of epidermal transfer cells in Vicia faba cotyledons. J. Exp. Bot. 63:3617–3629.

    CAS  Article  Google Scholar 

  3. Ansari, W.A., Atri, N., Singh, B., Pandey, S. 2016. Changes in antioxidant enzyme activities and gene expression in two muskmelon genotypes under progressive water stress. Biol. Plant. 61:333–341.

    Article  Google Scholar 

  4. Bradford, M.M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.

    CAS  Article  Google Scholar 

  5. Brennan, T., Frenkel, C. 1977. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol. 59:411–416.

    CAS  Article  Google Scholar 

  6. 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. 37:200.

    Article  Google Scholar 

  7. Dalton, D.A., Russell, S.A., Hanus, F.J., Pascoe, G.A., Evans, H.J. 1986. Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. Proc. Natl Acad. Sci. USA 83:3811–3815.

    CAS  Article  Google Scholar 

  8. Dringen, R. 2000. Glutathione metabolism and oxidative stress in neurodegeneration. Eur. J. Biochem. 267:4903.

    CAS  Article  Google Scholar 

  9. Grace, S.C., Logan, B.A. 1996. Acclimation of foliar antioxidant systems to growth irradiance in three broadleaved evergreen species. Plant Physiol. 112:1631–1640.

    CAS  Article  Google Scholar 

  10. Griffith, O.W. 1980. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106:207–212.

    CAS  Article  Google Scholar 

  11. Guajardo, E., Correa, J.A., Contreras-Porcia, L. 2016. Role of abscisic acid (ABA) in activating antioxidant tolerance responses to desiccation stress in intertidal seaweed species. Planta 243:767–781.

    CAS  Article  Google Scholar 

  12. Hodges, D.M., Andrews, C.J., Johnson, D.A., Hamilton, R.I. 1996. Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. Plant Physiol. 98:685–692.

    CAS  Article  Google Scholar 

  13. Hodges, M.D., DeLong, J.M., Forney, C.F., Prange, R.K. 1999. Improving the thiobarbituric acid-reactivesubstances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611.

    CAS  Article  Google Scholar 

  14. Jiang, M.Y., Zhang, J.H. 2002a. Role of abscisic acid in water stress-induced antioxidant defense in leaves of maize seedlings. Free Rad. Res. 36:1001–1015.

    CAS  Article  Google Scholar 

  15. Jiang, M.Y., Zhang, J.H. 2002b. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 53:2401–2410.

    CAS  Article  Google Scholar 

  16. Liu, Z.J., Guo, Y.K., Lin, S.H., Bai, J.G. 2009. Effects of exogenous hydrogen peroxide on ultra structure of chloroplasts and activities of antioxidant enzymes in greenhouse-ecotype cucumber under drought stress. Acta Horti. Sin. 36:1140–1146.

    CAS  Google Scholar 

  17. Miyake, C., Asada, K. 1992. Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. Plant Cell Physiol. 33:541–553.

    CAS  Google Scholar 

  18. Mohammadi, H., Moradi, F. 2016. Effects of growth regulators on enzymatic and non-enzymatic antioxidants in leaves of two contrasting wheat cultivars under water stress. Braz. J. Bot. 39:495–505.

    Article  Google Scholar 

  19. Mostofa, M.G., Fujita, M., Tran, L.S.P. 2015. Nitric oxide mediates hydrogen peroxide- and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul. 77:265–277.

    CAS  Article  Google Scholar 

  20. Nakano, Y., Asada, K. 1981. Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22:867–880.

    CAS  Google Scholar 

  21. Rüegsegger, A., Brunold, C. 1992. Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. Plant Physiol. 99:428–433.

    Article  Google Scholar 

  22. Sang, Q.Q., Shu, S., Shan, X., Guo, S.R. 2016. Effects of exogenous spermidine on antioxidant system of tomato seedlings exposed to high temperature stress. Russ. J. Plant Physiol. 63:645–655.

    CAS  Article  Google Scholar 

  23. Shan, C., Liang, Z. 2010. Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Plant Sci. 178:130–139.

    CAS  Article  Google Scholar 

  24. Singh, V.P., Singh, S., Kumar, J., Prasad, S.M. 2015. Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma 252:1217–1229.

    CAS  Article  Google Scholar 

  25. Tabata, K., Oba, K., Suzuki, K., Esaka, M. 2001. Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA of L-galactono-1,4-lactone dehydrogenase. Plant J. 27:139–148.

    CAS  Article  Google Scholar 

  26. Wang, Y., Zhang, J., Li, J.L., Ma, X. 2014. Exogenous hydrogen peroxide enhanced the thermotolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity. Acta Physiol. Plant. 36:2915–2924.

    CAS  Article  Google Scholar 

  27. Wheeler, G.L., Jones, M.A., Smirnoff, N. 1998. The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369.

    CAS  Article  Google Scholar 

  28. Wu, Z., Zhang, C., Yan, J., Yue, Q., Ge, Y. 2015. Effects of sulfur supply and hydrogen peroxide pretreatment on the responses by rice under cadmium stress. Plant Growth Regul. 77:299–306.

    CAS  Article  Google Scholar 

  29. Xing, X., Zhou, Q., Xing, H., Jiang, H., Wang, S. 2016. Early abscisic acid accumulation regulates ascorbate and glutathione metabolism in soybean leaves under progressive water stress. J. Plant Growth Regul. 35:865–876.

    CAS  Article  Google Scholar 

  30. Zhang, A., Jiang, M., Zhang, J., Ding, H., Xu, S., Hu, X., Tan, M. 2007. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol. 175:36–50.

    CAS  Article  Google Scholar 

  31. Zhao, L.Q., Zhang, F., Guo, J.K., Yang, Y.L., Li, B.B., Zhang, L.X. 2004. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134:849–857.

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Our study was funded by “Open project of Crop Science Characteristic Discipline of Henan Province” and “Important Science and Technology Specific Project of Henan Province (151100110700)”.

Author information

Affiliations

Authors

Corresponding author

Correspondence to C. Shan.

Additional information

Communicated by A. Pécsváradi

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Shan, C., Ou, X. Hydrogen Peroxide is Involved in the Regulation of Ascorbate and Glutathione Metabolism in Wheat Leaves under Water Stress. CEREAL RESEARCH COMMUNICATIONS 46, 21–30 (2018). https://doi.org/10.1556/0806.45.2017.053

Download citation

Keywords

  • water stress
  • hydrogen peroxide
  • ascorbate
  • glutathione
  • wheat