Biologia plantarum 62:188-193, 2018 | DOI: 10.1007/s10535-017-0740-9

Hydrogen sulfide is involved in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Arabidopsis thaliana

C. Shan1,2,3,4, T. Wang3,4, Y. Zhou1,3,4,*, W. Wang2
1 Postdoctoral Research Base, Henan Institute of Science and Technology, Xinxiang, P.R. China
2 Postdoctoral Research Centre, Henan Agricultural University, Zhengzhou, P.R. China
3 School of Science and Technology, Henan Institute of Science and Technology, Xinxiang, P.R. China
4 Collaborative Innovation Center of Modern Biological Breeding, Henan Province, Xinxiang, P.R. China

This study investigated the role of hydrogen sulfide (H2S) in the regulation of the ascorbate (AsA) and glutathione (GSH) metabolism by jasmonic acid (JA) in the leaves of Arabidopsis thaliana by using H2S scavenger hypotaurine (HT) and H2S synthetic mutant (SALK_041918, designated Atl-cdes). The results showed that JA significantly increased the H2S content, the activities of L-cysteine desulfhydrase (L-CDes), D-cysteine desulfhydrase (D-CDes), ascorbate peroxidase (APX), glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), L-galactono-1,4-lactone dehydrogenase (GalLDH) and γ-glutamylcysteine synthetase (γ-ECS), the ratio of AsA to dehydroascorbate (DHA), and decreased the content of malondialdehyde (MDA) and H2O2 in the wild type of A. thaliana, compared to control. The above effects of JA except the increased activities of L-CDes and D-CDes were suppressed by addition of HT. However, JA and HT+JA had no significant effects on the ratio of reduced GSH to oxidized GSH (GSSG) in the wild type of A. thaliana. Application of HT to the control decreased H2S content, AsA/DHA ratio, and activities of APX, GR, DHAR, MDHAR, γ-ECS, and GalLDH, but had no effects on MDA content, activities of L-CDes and D-CDes, and GSH/GSSG ratio. In the H2S synthetic mutant, JA had no obvious effects on above mentioned parameters except the D-CDes activity compared with the control. Our results suggest that JA-induced H2S, which is a signal that leads to the up-regulation of the AsA and GSH metabolism.

Keywords: ascorbate peroxidase; cysteine desulfhydrase; glutathione reductase; H2S synthetic mutant; hypotaurine
Subjects: hydrogen sulfide; jasmonic acid; ascorbic acid; glutathione; malondialdehyde; hydrogen peroxide; ascorbate peroxidase
Species: Arabidopsis thaliana

Received: September 30, 2016; Revised: March 12, 2017; Accepted: March 15, 2017; Published: January 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Shan, C., Wang, T., Zhou, Y., & Wang, W. (2018). Hydrogen sulfide is involved in the regulation of ascorbate and glutathione metabolism by jasmonic acid in Arabidopsis thaliana. Biologia plantarum62(1), 188-193. doi: 10.1007/s10535-017-0740-9.
Download citation

References

  1. Bradford, M.M.: 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, 1976. Go to original source...
  2. Chen, J., Shang, Y.T., Wang, W.H., Chen, X.Y., He, E.M., Zheng, H.L., Shangguan Z.: Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. - Front. Plant Sci. 7: 1-18, 2016. Go to original source...
  3. Chen, J., Wang, W.H., Wu, F.H., You, C.Y., Liu, T.W., Dong, X.J., He, J.X., Zheng, H.L.: Hydrogen sulfide alleviates aluminum toxicity in barley seedlings. - Plant Soil 362: 301-318, 2013. Go to original source...
  4. Dalton, D.A., Russell, S.A., Hanus, F.J., Pascoe, G.A., Evans, H.J.: Enzymatic reactions of ascorbate and glutathione that prevent peroxide damage in soybean root nodules. - Proc. nat. Acad. Sci. USA 83: 3811-3815, 1986. Go to original source...
  5. Grace, S.C., Logan, B.A.: Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species. - Plant Physiol. 112: 1631-1640, 1996. Go to original source...
  6. Griffith, O.W.: Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. - Anal. Biochem. 106: 207-212, 1980. Go to original source...
  7. Hodges, M.D., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. - Planta 207: 604-611, 1999. Go to original source...
  8. Hodges, D.M., Andrews, C.J., Johnson, D.A., Hamilton, R.I.: Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. - Physiol. Plant. 98: 685-692, 1996. Go to original source...
  9. Hou, Z.H., Liu, J., Hou, L.X., Li, X.D., Liu, X.: H2S may function downstream of H2O2 in jasmonic acid-induced stomatal closure in Vicia faba. - Chin. Bull. Bot. 46: 396-406, 2011.
  10. Li, L., Wang, Y., Shen, W.: Roles of hydrogen sulfide and nitric oxide in the alleviation of cadmium-induced oxidative damage in alfalfa seedling roots. - Biometals 25: 617-631, 2012. Go to original source...
  11. Li, Z.G., Gu, S.P.: Hydrogen sulfide as a signal molecule in hematin-induced heat tolerance of tobacco cell suspension. - Biol. Plant. 60: 595-600, 2016. Go to original source...
  12. Liu, J., Hou, L.X., Liu, G.H., Liu, X., Wang, X.C.: Hydrogen sulfide induced by nitric oxide mediates ethylene-induced stomatal closure of Arabidopsis thaliana. - Chin. Sci. Bull. 56: 2515-2522, 2011. Go to original source...
  13. Miyake, C., Asada, K.: Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids. - Plant Cell Physiol. 33: 541-553, 1992.
  14. Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
  15. Noctor, G., Foyer, C.H.: Ascorbate and glutathione: keeping active oxygen under control. - Annu. Rev. Plant Physiol. 49: 249-279, 1998. Go to original source...
  16. Okuda, T., Masuda, Y., Yamanka, A., Sagisaka, S.: Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. - Plant Physiol. 97: 1265-1267, 1991. Go to original source...
  17. Peng, R., Bian, Z., Zhou, L., Cheng, W., Hai, N., Yang, C., Yang, T., Wang, X., Wang, C.: Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L.). - Plant Cell Rep. 35: 2325-2340, 2016. Go to original source...
  18. Radhika, V., Kost, C., Boland, W., Heil, M.: The Role of jasmonates in floral nectar secretion. - PloS ONE 5: 9265, 2010. Go to original source...
  19. Ren, C., Dai, C.: Jasmonic acid is involved in the signaling pathway for fungal endophyte-induced volatile oil accumulation of Atractylodes lancea plantlets. - BMC Plant Biol. 12: 128-133, 2012. Go to original source...
  20. Riemenschneider, A., Nikiforova, V., Hoefgen, R., Papenbrock, J.: Impact of elevated H2S on metabolite levels, activity of enzymes and expression of genes involved in cysteine metabolism. - Plant Physiol. Biochem. 43: 473-483, 2005. Go to original source...
  21. Rüegsegger, A., Brunold, C.: Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. - Plant Physiol. 99: 428-433, 1992. Go to original source...
  22. Shan, C., Liang, Z.: Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. - Plant Sci. 178: 130-139, 2010. Go to original source...
  23. Shan, C., Liang, Z., Sun, Y., Hao, W., Han, R.: The protein kinase MEK1/2 participates in the regulation of ascorbate and glutathione content by jasmonic acid in Agropyron cristatum leaves. - J. Plant Physiol. 168: 514-518, 2011a. Go to original source...
  24. Shan, C., Zhang, S., Li, D., Zhao, Y., Tian, X., Zhao, X., Wu, Y., Wei, X., Liu, R. Effects of exogenous hydrogen sulfide on the ascorbate and glutathione metabolism in wheat seedlings leaves under water stress. - Acta Physiol. Plant. 33: 2533-2540, 2011b. Go to original source...
  25. Shan, C., Zhou, Y., Liu, M.: Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. - Protoplasma 252: 1397-1405, 2015. Go to original source...
  26. Wang, L., Hou, Z., Hou, L., Zhao, F., Liu, X.: H2S induced by H2O2 mediates drought-induced stomatal closure in Arabidopsis thaliana. - Chin. Bull. Bot. 47: 217-225, 2012.
  27. Yamasaki, H., Cohen, M.F.: Biological consilience of hydrogen sulfide and nitric oxide in plants: gases of primordial earth linking plant, microbial and animal physiologies. - Nitric Oxide 55-56: 91-100, 2016. Go to original source...
  28. Zhang, H., Hu, L.Y., Hu, K.D., He, Y.D., Wang, S.H., Luo, J.P.: Hydrogen sulfide promotes wheat seed germination and alleviates the oxidative damage against copper stress. - J. Integr. Plant Biol. 50: 1518-1529, 2008. Go to original source...
  29. Zhang, H., Hu, L.Y., Li, P., Hu, K.D., Jiang, C.X., Luo, J.P.: Hydrogen sulfide alleviated chromium toxicity in wheat. - Biol. Plant. 54: 743-747, 2010b. Go to original source...
  30. Zhang, H., Tang, J., Liu, X.P., Wang, Y., Yu, W., Peng, W.Y., Fang, F., Ma, D.F., Wei, Z.J., Hu, L.Y.: Hydrogen sulfide promotes root organogenesis in Ipomoea batatas, Salix matsudana and Glycine max. - J. Integr. Plant Biol. 51: 1086-1094, 2009a. Go to original source...
  31. Zhang, H., Wang, M.J., Hu, L.Y., Wang, S.H., Hu, K.D., Bao, L.J., Luo, J.P.: Hydrogen sulfide promotes wheat seed germination under osmotic stress. - Russ. J. Plant Physiol. 57: 532-539, 2010a. Go to original source...
  32. Zhang, H., Ye, Y.K., Wang, S.H., Luo, J.P., Tang, J., Ma, D.F.: Hydrogen sulfide counteracts chlorophyll loss in sweetpotato seedling leaves and alleviates oxidative damage against osmotic stress. - Plant Growth Regul. 58: 243-250, 2009b. Go to original source...
  33. Ziogas, V., Tanou, G., Belghazi, M., Filippou, P., Fotopoulos, V., Grigorios, D., Molassiotis, A.: Roles of sodium hydrosulfide and sodium nitroprusside as priming molecules during drought acclimation in citrus plants. - Plant mol. Biol. 89: 433-450, 2015. Go to original source...