Abstract
Magnesium (Mg) deficiency in plants is a widespread problem, affecting productivity and quality in agriculture. The mechanism of Mg deficiency inducing antioxidant enzyme activities has not been elucidated in rice. We examined the relationship among abscisic acid (ABA), H2O2, and antioxidant enzymes in the leaves of rice seedlings grown under conditions of Mg deficiency. The expression of OsRab16A, an ABA responsive gene, was used to determine the content of ABA. Mg deficiency resulted in increased ABA content in leaves of rice seedlings. The production of H2O2 was examined by 3,3-diaminobenzidine staining and a colorimetric method. Mg deficiency also induced H2O2 production in leaves, which was blocked by dipehnyleneiodonium chloride (DPI), an NADPH oxidase inhibitor. Tungstate (Tu), an ABA biosynthesis inhibitor, was effective in reducing Mg deficiency-increased ABA content, as well as Mg deficiency-induced H2O2 production. Both Tu and DPI were effective in reducing Mg deficiency-induced activities of superoxide dismutase, ascorbate peroxidase, glutathione reductase, and catalase in the leaves. Mg deficiency-induced ABA accumulation may trigger increased production of H2O2, which may involve plasma-membrane NADPH oxidase, and, in turn, up-regulates the activities of antioxidant enzymes in leaves of rice seedlings.
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Abbreviations
- ABA:
-
Abscisic acid
- APX:
-
Ascorbate peroxidase
- AsA:
-
Ascorbic acid
- CAT:
-
Catalase
- DAB:
-
3,3-Diaminobenzidine
- DPI:
-
Diphenyleneiodonium chloride
- FM:
-
Fresh mass
- GR:
-
Glutathione reductase
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- Tu:
-
Sodium tungstate
References
Aitken RL, Dickson T, Hailes KJ, Moody PW (1999) Response of field-grown maize to applied magnesium in acidic soil in north eastern Australia. Aust J Agric Res 1999:191–198
Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosyn Res 60:43–73
Bolwell GP, Davies DR, Gerrish C, Auh CK, Mrphy TM (1998) Comparative biochemistry of the oxidative burst produced by rose and Frenc bean cells reveals two distinct mechanisms. Plant Physiol 116:1374–1385
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal Biochem 72:248–254
Bueno P, Piqueras A, Kurepa J, Savouré A, Verbruggen N, Van Montagu M, Inzé D (1998) Expression of antioxidant enzymes in response to abscisic and high osmoticum in tobacco BY- cell cultures. Plant Sci 138:27–34
Cakmak I, Kirby EA (2008) Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 131:692–704
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227
Chou T-S, Chao Y–Y, Huang W-D, Hong C-Y, Kao CH (2011) Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedling. J Plant Physiol doi:10.1016/j.jplph.2010.12.004
Ding Y-C, Chang C-R, Luo W, Wu Y-S, Ren X-L, Wang P, Xu G-H (2008) High potassium aggravates the oxidative stress induced by magnesium deficiency in rice leaves. Pedosphere 18:316–327
Foster JG, Hess JL (1980) Responses of superoxide dismutase and glutathione reductase activities in cotton leaf tissue exposed to an atmosphere enriched in oxygen. Plant Physiol 166:482–487
Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara coralline: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066
Hermans C, Johnson GN, Strasser RJ, Verbruggen M (2004) Physiological characterization of magnesium deficiency in sugar beet: acclimation to low magnesium differentially affects photosystems I and II. Planta 220:344–355
Hermans C, Vuylsreke M, Coppens F, Cristrescu SM, Harren FJM, Inzé D (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Ababidopsis thaliana. New Phytol 187:132–144
Hong C-Y, Chao Y–Y, Yang M-Y, Cheng S-Y, Cho S-C, Kao CH (2009) NaCl-indued expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant Soil 320:103–115
Hsu YT, Kao CH (2007) Toxicity in leaves of rice exposed to cadmium is due to hydrogen peroxide accumulation. Plant Soil 298:231–241
Hu X, Zhang A, Zheng J, Jiang M (2006) Abscisic acid is a key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495
Hung KT, Kao CH (2004) Hydrogen peroxide is necessary for abscisic acid-induced senescence of rice leaves. J Plant Physiol 161:1347–1357
Jannat R, Uraji M, Morofuji M, Islam MM, Bloom RE, Nakmura Y, McClung CR, Schroeder JI, Mori IC, Murata Y (2011) Roles of intracellular hydrogen peroxide accumulation in abscisic acid signaling in Arabidopsis guard cells. J Plant Physiol doi:10.1016/j.jplph.2011.05.006
Jiang M, Zhang J (2002) 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
Kato M, Shimizu S (1987) Chlorophyll metabolism in higher plants. VII. Chlorophyll degradation in senescing tobacco leaves: phenolic-dependent peroxidative degradation. Can J Bot 65:729–735
Kimura J (1931) Responses of rice plants to mineral nutrients in a culture solution in comparison with those of barley and wheat. J Imper Agri Exp Sta 1:375–402
Lee H-S, Milborrow BV (1997) Endogenous biosynthetic precursor of (+)-abscisic acid. V. Inhibition by tungstate and its removal by Cinchonine shows that xanthoxal is oxidized by molybdo-aldehyde oxidase. Aus J Plant Physiol 24:727–732
Lin CC, Kao CH (2001) Abscisic acid induced changes in cell wall peroxidase activity and hydrogen peroxide level in roots of rice seedlings. Plant Sci 160:323–329
Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138
Mengel K, Kirby EA (1987) Principle of plant nutrition. International Potash Institute, Worblaufen-Bern
Mizarhi Y, Richmond AE (1972) Abscisic acid in relation to mineral deprivation. Plant Physiol 50:667–670
Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279–2286
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432
Paoletti F, Aldinucci D, Mocali A, Capparini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154:536–541
Pei ZM, Murata N, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734
Quan L-J, Zhang B, Shi W–W, Li H-Y (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integr Plant Biol 50:2–18
Tewari RK, Kumar P, Sharma PN (2006) Magnesium deficiency induced oxidative stress and antioxiant responses in mulberry plants. Sci Hort 108:7–14
Tsai Y-C, Kao CH (2004) The involvement of hydrogen peroxide in abscisic acid-induced activities of ascorbae peroxidase and glutathione reductase in rice roots. Plant Growth Regul 43:207–212
Tsai Y-C, Hong C-Y, Liu L-F, Kao CH (2004) Relative importance of Na+ and Cl− in NaCl-induced antioxidant systems in roots or rice seedlings. Physiol Plant 122:86–94
Vysotskaya LB, Korobova AV, Kudoyarova GR (2008) Abscisic acid accumulation in the roots of nutrient-limited plants: its impact on the differential growth of roots and shoots. J Plant Physiol 165:1274–1279
Wind S, Beuerlein K, Eucker T, Műller H, Scheurer P, Armitage ME, Ho H, Schmidt HHHW, Wingler K (2010) Comparative pharmacology of chemically distinct NADPH oxidase inhibitors. Br J Pharmacol 161:885–898
Zabadal TJ (1974) A water potential threshold for the increase of abscisic acid in leaves. Plant Physiol 53:125–127
Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song C-P (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
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This work was supported by a research grant from the National Science Council of the Republic of China.
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Chao, YY., Chou, TS. & Kao, C.H. Involvement of abscisic acid and hydrogen peroxide in regulating the activities of antioxidant enzymes in leaves of rice seedlings under magnesium deficiency. Plant Growth Regul 66, 1–8 (2012). https://doi.org/10.1007/s10725-011-9623-9
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DOI: https://doi.org/10.1007/s10725-011-9623-9