Abstract
This study investigated the regulation of ascorbate and glutathione metabolism by nitric oxide in Agropyron cristatum leaves under water stress. The activities of 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), and the contents of NO, reduced ascorbic acid (AsA), reduced glutathione (GSH), total ascorbate and total glutathione increased under water stress. These increases were suppressed by pretreatments with NO synthesis inhibitors N G-nitro-L-arginine methyl ester (L-NAME) and 4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO). However, application of L-NAME and cPTIO to plants sufficiently supplied with water did not affect the activities of above mentioned enzymes and the contents of NO and above mentioned antioxidants. Pretreatments with L-NAME and cPTIO increased the malondialdehyde (MDA) content and electrolyte leakage of plants under water stress. Our results suggested that water stress-induced NO is a signal that leads to the upregulation of ascorbate and glutathione metabolism and has important role for acquisition of water stress tolerance.
Abbreviations
- APX:
-
ascorbate peroxidase
- AsA:
-
reduced ascorbic acid
- DHAR:
-
dehydroascorbate reductase
- γ-ECS:
-
γ-glutamylcysteine synthetase
- GalLDH:
-
L-galactono-1,4-lactone dehydrogenase
- GR:
-
glutathione reductase
- GSH:
-
reduced glutathione
- MDA:
-
malondialdehyde
- MDHAR:
-
monodehydroascorbate reductase
- L-NAME-N G :
-
nitro-L-arginine methyl ester
- cPTIO:
-
4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide
References
Apel, K., Hirt, H.: Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. — Annu. Rev. Plant Biol. 55: 373–399, 2004.
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.
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.
Dringen, R.: Glutathione metabolism and oxidative stress in neurodegeneration. — Eur. J. Biochem. 267: 4903, 2000.
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.
Griffith, O.W.: Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. — Anal. Biochem. 106: 207–212, 1980.
Guo, F.Q., Crawford, N.M.: Arabidopsis nitric oxide synthase 1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. — Plant Cell 17: 3436–3450, 2005.
Hodges, D.M., Andrews, C.J., Johnson, D.A., Hamilton, R.I.: Antioxidant compound responses to chilling stress in differentially sensitive inbred maize lines. — Plant Physiol. 98: 685–692, 1996.
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.
Hu, W.H., Xiao, Y.A., Zeng, J.J., Hu, X.H.: Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. — Biol. Plant. 54: 761–765, 2010.
Hu, X., Neill, S.J., Tang, Z., Cai, W.: Nitric oxide mediates gravitropic bending in soybean roots. — Plant Physiol. 137: 663–670, 2005.
Jiang, M.Y., Zhang, J.H.: 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, 2002.
Lan, Y.P., Han, Z.H., Xu, X.F.: Accumulation of jasmonic acid in apple seedlings under water stress. — Acta hort. sin. 31: 16–20, 2004.
Li, L., Van Staden, J., Jäger, A.K.: Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. — Plant Growth Regul. 25: 81–87, 1998.
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.
Mýtinová, Z., Motyka, V., Haisel, D., Gaudinová, A., Lubovská, Z., Wilhelmová, N.: Effect of abiotic stresses on the activity of antioxidative enzymes and contents of phytohormones in wild type and AtCKX2 transgenic tobacco plants. — Biol. Plant. 54: 461–470, 2010.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. — Plant Cell Physiol. 22: 867–880, 1981.
Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J.: Nitric oxide, stomatal closure, and abiotic stress. — J. exp. Bot. 59: 165–176, 2008.
Noctor, G., Foyer, C.H.: Ascorbate and glutathione: keeping active oxygen under control. — Annu. Rev. Plant Physiol. 49: 249–279, 1998.
Pagnussat, G.C., Lanteri, M.L., Lombardo, M.C., Lamattina, L.: Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. — Plant Physiol. 135: 279–286, 2004.
Ruan, H.H., Shen, W.B., Liu, K.L., Xu, L.L.: Effects of exogenous NO donor on glutathione-dependent antioxidative system in wheat seedling leaf under salt stress. — Acta agron. sin. 31: 1144–1149, 2005.
Rüegsegger, A., Brunold, C.: Effect of cadmium on γ-glutamylcysteine synthesis in maize seedlings. — Plant Physiol. 99: 428–433, 1992.
Shan, C., Liang, Z.: Jasmonic acid regulates ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. — Plant Sci. 178: 130–139, 2010.
Song, L.L., Ding, W., Shen, J., Zhang, Z.G., Bi, Y.R., Zhang, L.X.: Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. — Plant Sci. 175: 826–832, 2008.
Vuletić, M., Šukalović, V.H., Marković, K., Maksimović, J.D.: Antioxidative system in maize roots as affected by osmotic stress and different nitrogen sources. — Biol. Plant. 54: 530–534, 2010.
Wang, Y., Lin, J.S., Wang, G.X.: Role of calcium in nitric oxide-induced programmed cell death in tobacco protoplasts. — Biol. Plant. 54: 471–476, 2010.
Wheeler, G.L., Jones, M.A., Smirnoff, N.: The biosynthetic pathway of vitamin C in higher plants. — Nature 393: 365–369, 1998.
Wu, J.C., Chen, J.Q., Liang, J., Yang, W.B., Wu, J.J., Chen, L.Q., Liu, M.Q., Chen, L.Q.: Effects of exogenous NO on ascorbate-glutathione cycle in loquat leaves under low temperature stress. — Chin. J. appl. Ecol. 20: 1395–1400, 2009.
Zeier, J., Delledonne, M., Mishina, T., Severi, E., Sonoda, M., Lamb, C.: Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. — Plant Physiol. 136: 2875–2886, 2004.
Zhang, A., Jiang, M., Zhang, J., Ding, H., Xu, S., Hu, X., Tan, M.: 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, 2007.
Zhao, L.Q., Zhang, F., Guo, J.K., Yang, Y.L., Li, B.B., Zhang, L.X.: Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. — Plant Physiol. 134: 849–857, 2004.
Zottini, M., Formentin, E., Scattolin, M., Carimi, F., Lo Schiavo, F., Terzi, M.: Nitric oxide affects plant mitochondrial functionality in vivo. — FEBS Lett. 515: 75–78, 2002.
Acknowledgements
We appreciated financial support by the Knowledge Innovation Program of the Chinese Academy of Science (KZCX2-YW-443), National Scientific and Technological Support Program of the Ministry of Science and Technology of China (2008BAD98B08) and Personnel Foundation of Northwest A & F University. The first two authors contributed equally to this paper.
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Shan, C., He, F., Xu, G. et al. Nitric oxide is involved in the regulation of ascorbate and glutathione metabolism in Agropyron cristatum leaves under water stress. Biol Plant 56, 187–191 (2012). https://doi.org/10.1007/s10535-012-0040-3
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DOI: https://doi.org/10.1007/s10535-012-0040-3