Biologia plantarum 56:313-320, 2012 | DOI: 10.1007/s10535-012-0092-4

Role of hydrogen peroxide in regulating glucose-6-phosphate dehydrogenase activity under salt stress

Y. Liu1,2, Q. Wan1, R. Wu1, X. Wang1, H. Wang3, Z. Wang3, C. Shi3, Y. Bi1,*
1 School of Life Sciences, Lanzhou University, Lanzhou, P.R. China
2 College of Life Sciences, Shandong Agricultural University, Taian, P.R. China
3 College of Life and Environmental science, Minzu University of China, Beijing, P.R. China

The role of hydrogen peroxide in the regulation of glucose-6-phosphate dehydrogenase (G6PDH) activity in the red kidney bean (Phaseolus vulgaris L.) roots under salt stress (100 mM NaCl) was investigated. Salt stress caused the increase of the activities of G6PDH and antioxidative enzymes including ascorbate peroxidase (APX), catalase (CAT), peroxidase (POD), superoxide dismutase (SOD), as well as H2O2 production. The application of H2O2 (1 mM) also enhanced the activities of G6PDH as well as antioxidative enzymes. In the presence of exogenous CAT, H2O2 content was decreased, and the enhanced activities of G6PDH and antioxidative enzymes induced by NaCl or by exogenous H2O2 were also abolished, suggesting that the enhancement of the above enzyme activities under salt stress was a result of the increased endogenous H2O2 levels. Further results showed that the effects of NaCl and H2O2 on the activities of antioxidative enzymes were diminished by Na3PO4 (a G6PDH inhibitor), suggesting G6PDH activity is required in enhancing the activities of antioxidative enzymes. The enhanced membrane leakage, lipid peroxidation, H2O2 and O2 - contents, G6PDH and antioxidative enzyme activities under salt stress were all recovered to control level when the red kidney bean seedlings treated with 100 mM NaCl for 6 d were transferred to the control conditions for 8 d.

Keywords: antioxidative enzymes; NaCl; Phaseolus vulgaris; red kidney bean; redox status
Subjects: antioxidative enzymes; NaCl; redox status; hydrogen peroxide; glucose-6-phosphate dehydrogenase; ascorbate peroxidase; peroxidase; catalase; superoxide dismutase; Western blot

Received: December 14, 2009; Accepted: December 9, 2010; Published: June 1, 2012Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Liu, Y., Wan, Q., Wu, R., Wang, X., Wang, H., Wang, Z., Shi, C., & Bi, Y. (2012). Role of hydrogen peroxide in regulating glucose-6-phosphate dehydrogenase activity under salt stress. Biologia plantarum56(2), 313-320. doi: 10.1007/s10535-012-0092-4.
Download citation

References

  1. Adam, A.L., Bestwick, C.S., Barna, B., Mansfield, J.W.: Enzymes regulating the accumulation of active oxygen species during the hypersensitive reaction of bean to Pseudomonas syringae pv. phaseolicola. - Planta 197: 240-249, 1995.
  2. Aebi, H.: Catalase in vitro. - Methods Enzymol. 105: 121-126, 1984. Go to original source...
  3. Apel, K., Hirt, H.: Reactive oxygen species: metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
  4. Bartosz, G.: Oxidative stress in plants. - Acta Physiol. Plant 19: 47-64, 1997. Go to original source...
  5. Batz, O., Logemann, E., Reinold, S., Hahlbrock, K.: Extensive reprogramming of primary and secondary metabolism by fungal elicitor or infection in parsley cells. - Biol. Chem. 379: 1127-1135, 1998. Go to original source...
  6. Bi, Y.R., Liang, H.G.: Changes of respiratory metabolism pathway during the tissue differentiation and bud formation in tobacco callus cultures. - Acta biol. Exp. sin. 20: 109-117, 1987.
  7. Cai, J., Jones, D.P.: Mitochondrial redox signaling during apoptosis. - J. Bioenerg. Biomembr. 31: 327-334, 1999. Go to original source...
  8. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., Van Breusegem, F.: Dual action of the active oxygen species during plant stress responses. - Cell. mol. Life Sci. 57: 779-795, 2000. Go to original source...
  9. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver D.J., Coutu, J., Shulaev, V., Schlauch, K., Mittler, R.: Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. - Plant Cell 17: 268-281, 2005. Go to original source...
  10. Debnam, P.M., Fernie, A.R., Leisse, A., Golding, A., Bowsher, C.G.., Grimshaw, C., Knight, J.S., Emes, M.J.: Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. - Plant J. 38: 49-59, 2004. Go to original source...
  11. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chétrit, P., Foyer, C.H., Paepe, R.: Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. - Plant Cell 15: 1212-1226, 2003. Go to original source...
  12. Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase. - Anal. Biochem. 70: 616-620, 1976. Go to original source...
  13. Esposito, S., Carfagna, S., Massaro, G., Vona, V., Di, M.R.V.: Glucose-6-phosphate dehydrogenase in barley roots: kinetic properties and localization of the isoforms. - Planta 212: 627-634, 2001. Go to original source...
  14. Esposito, S., Carillo, E., Carfagna, S.: Ammonium metabolism stimulation of glucose-6-phosphate dehydrogenase and phosphoenolpyruvate carboxylase in young barley roots. - J. Plant Physiol. 153: 61-66, 1998. Go to original source...
  15. Fedina, I.S., Nedeva, D., Çiçek, N.: Pre-treatment with H2O2 induces salt tolerance in barley seedlings. - Biol. Plant. 53: 321-324, 2009. Go to original source...
  16. Foyer, C.H., Noctor, G.: Oxygen processing in photosynthesis: regulation and signalling. - New Phytol. 146: 359-388, 2000. Go to original source...
  17. Foyer, C.H., Noctor, G.: Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. - Plant Cell 17: 1866-1875, 2005a.
  18. Foyer, C.H., Noctor, G.: Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. - Plant Cell Environ. 28: 1056-1071, 2005b. Go to original source...
  19. Frew, J., Jones, P., Scholes, G..: Spectrophotometric determination of hydrogen peroxide and organic hydroperoxides at low concentrations in aqueous solution. - Anal. chim. Acta 155: 130-150, 1983. Go to original source...
  20. Fridovich, I.: Biological effects of the superoxide radical. - Arch. Biochem. Biophys. 247: 1-11, 1986. Go to original source...
  21. Groten, K., Vanacker, H., Dutilleul, C., Bastian, F., Bernard, S., Carzaniga, R., Foyer, C.H.: The roles of redox processes in pea nodule development and senescence. - Plant Cell Environ. 28: 1293-1304, 2005. Go to original source...
  22. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., Bohnert, H.J.L.: Plant cellular and molecular responses to high salinity. - Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 463-499, 2000. Go to original source...
  23. Hauschild, R., Schaewen, A.V.: Differential regulation of glucose-6-phosphate dehydrogenase isoenzyme activities in potato. - Plant Physiol. 133: 47-62, 2003. Go to original source...
  24. Hernández, J.A., Corpas, F.J., Gómez, M., Del Río, L.A., Sevilla, F.: Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. - Physiol. Plant. 89: 103-110, 1993. Go to original source...
  25. Hernández, J.A., Del Rio, L.A., Sevilla, F.: Salt stress-induced changes in superoxide dismutase isozymes in leaves and mesophyll protoplasts from Vigna unguiculata L. Walp. - New Phytol. 126: 37-44, 1994. Go to original source...
  26. Hernández, J.A., Olmos, E., Corpas, F.J., Sevilla, F., Del Río, L.A.: Salt-induced oxidative stress in chloroplasts of pea plants. - Plant Sci. 105: 151-167, 1995. Go to original source...
  27. Hilal, M., Zenoff, A.M., Ponessa, G., Moreno, H., Massa, E.M.: Saline stress alters the temporal patterns of xylem differentiation and alternative oxidase expression in developing soybean roots. - Plant Physiol. 117: 695-701, 1998. Go to original source...
  28. Hodges, D.M., 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...
  29. Janda, T., Szalai, G., Tari, I., Paldi, E.: Hydroponic treatment with salicylic acid decreases the effects of chilling in maize (Zea mays L.) plants. - Planta 208: 175-180, 1999. Go to original source...
  30. Kruse, E., Mock, H.P., Grimm, B.: Reduction of coproporphyrinogen oxidase level by antisense RNA synthesis leads to deregulated gene expression of plastid proteins and affects the oxidative stress defense system. - EMBO J. 14: 3712-3737, 1995. Go to original source...
  31. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. - Nature 227: 680-685, 1970. Go to original source...
  32. Liu, Y.G., Wu, R.R., Wan, Q., Xie, G.Q., Bi, Y.R.: Glucose-6-phosphate dehydrogenase plays a pivotal role in nitric oxide-involved defense against oxidative stress under salt stress in red kidney bean roots. - Plant Cell Physiol. 48: 511-522, 2007. Go to original source...
  33. Logemann, E., Tavernaro, A., Schulz, W., Somssich, I.E., Hahlbrock, K.: UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. - Proc. nat. Acad. Sci. USA 97: 1903-1907, 2000.
  34. Maia, J.M., Costa de Macedo, C.E., Voigt, E.L., Freitas, J.B.S., Silveira, J.A.G.: Antioxidative enzymatic protection in leaves of two contrasting cowpea cultivars under salinity. - Biol. Plant. 54: 159-163, 2010. Go to original source...
  35. Mittler, R.: Oxidative stress, antioxidants and stress tolerance. - Trends Plant Sci. 7: 405-410, 2002. Go to original source...
  36. Mullineaux, P., Karpinski, S.: Signal transduction in response to excess light: getting out of the chloroplast. - Curr. Opin. Plant Biol. 5: 43-48, 2002. Go to original source...
  37. Mutlu, S., Atici, Ö., Nalbantoglu, B.: Effects of salicylic acid and salinity on apoplastic antioxidant enzymes in two wheat cultivars differing in salt tolerance. - Biol. Plant. 53: 334-338, 2009. Go to original source...
  38. Neill, S.J., Desikan, R., Clarke, A., Hancock, J.T.: Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. - Plant Physiol. 128: 13-16, 2002. Go to original source...
  39. Nemoto, Y., Sasakuma, T.: Specific expression of glucose-6-phosphate dehydrogenase (G6PDH) gene by salt stress in wheat (Triticum aestivum L.). - Plant Sci. 158: 53-60, 2000. Go to original source...
  40. Pugin, A., Frachisse, J.M., Tavernier, E., Bligny, R., Gout, E., Douce, R., Guern, J.: Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. - Plant Cell 9: 2077-2091, 1997. Go to original source...
  41. Sairam, R.K., Srivastava, G.C.: Changes in antioxidant activity in subcellular fraction of tolerant and susceptible wheat genotypes in response to long term salt stress. - Plant Sci. 162: 897-904, 2002. Go to original source...
  42. Shen, S.C., Chen, J.P.: Pentose metabolism and the influence of orthophosphate on the paths of sugar degradation of Streptomyces aureofaciens. - Sci. sin. 8: 733-746, 1959.
  43. Šindelář, L., Šindelářová, M.: Correlation of viral RNA biosynthesis with glucose-6-phosphate dehydrogenase activity and host resistance. - Planta 215: 862-869, 2002.
  44. Song, L.L., Ding, W., Zhao, M.G., Sun, B.T., Zhang, L.X.: Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. - Plant Sci. 171: 449-458, 2006. Go to original source...
  45. Tecsi, L.I., Maule, A.J., Smith, A.M., Leegood, R.C.: Metabolic alterations in cotyledons of Cucurbita pepo infected by cucumber mosaic virus. - J. exp. Bot. 45: 1541-1551, 1994. Go to original source...
  46. Tian, W.N., Braunstein, L.D., Pang, J., Stuhlmeier, K.M., Xi, Q.C., Tian, X., Stanton, R.C.: Importance of glucose-6-phosphate dehydrogenase activity for cell growth. - J. biol. Chem. 273: 10609-10617, 1998. Go to original source...
  47. Vuletić, M., HadŽi-Tašković Šukalović, V., Marković, K., Dragišić Maksimović, J.: Antioxidative system in maize roots as affected by osmotic stress and different nitrogen sources. - Biol. Plant. 54: 530-534, 2010. Go to original source...
  48. Wang, X.M., Ma, Y.Y., Huang, C.H., Wan, Q., Li, N., Bi, Y.R.: Glucose-6-phosphate dehydrogenase plays a central role in modulating reduced glutathione levels in reed callus under salt stress. - Planta 227: 611-623, 2008a. Go to original source...
  49. Wang, X.M., Ma, Y.Y., Huang, C.H., Li, J.S., Wan, Q., Li, N., Bi, Y.R.: Involvement of glucose-6-phosphate dehydrogenase in reduced glutathione maintenance and hydrogen peroxide signal under salt stress. - Plant Signaling Behavior 3: 394-395, 2008b. Go to original source...
  50. Xing, Y., Jia, W.S., Zhang, J.H.: AtMEK1 mediates stressinduced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. - J. exp. Bot. 58: 2969-2681, 2007. Go to original source...
  51. Yu, L.J., Lan, W.Z., Chen, C., Yang, Y.: Glutathione levels control glucose-6-phosphate dehydrogenase activity during elicitor-induced oxidative stress in cell suspension cultures of Taxus chinensis. - Plant Sci. 167: 329-335, 2004. Go to original source...
  52. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Tan, M.P., Hu, X.L.: Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. - Plant Physiol. 141: 475-487, 2006. Go to original source...
  53. Zhang, A.Y., Jiang, M.Y., Zhang, J.H., Ding, H.D., Xu, S.C., Hu, X.L., Tan, M.P.: 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: 35-60, 2007. Go to original source...