Abstract
Endogenous salicylic acid (SA) functions in plant response to an aluminum stress were assessed. We used different Arabidopsis thaliana genotypes including snc1 with a constitutively high content of SA, sid2 and nahG (transgenic lines) both with a low content of SA, SA insensitive mutant npr1-1, and snc1/nahG (i.e., the nahG expression in the snc1 background) with a similar SA content as in wild type (WT) plants. Results show that the snc1 plants displayed obvious growth retardation of roots and shoots under the Al3+ stress, whereas the sid2, nahG, and npr1-1 plants exhibited alleviated symptoms in comparison with the WT plants. The Al3+ content increased in all the tested genotypes with the increasing AlCl3 concentration applied, but no significant variations were detected among the tested genotypes. The snc1 had much higher superoxide dismutase and peroxidase activities, and a lower catalase activity and the ratio of reduced to oxidized glutathione accompanied by higher accumulations of H2O2 and malondialdehyde compared with the WT plants. These changes were largely reversed by the introduction of nahG; the sid2, nahG, and npr1-1 plants were less affected than WT plants in all the above-mentioned parameters. The Al3+ stress significantly enhanced malate exudation in all the tested genotypes, but no significant correlation was observed between the SA-involved response to the Al3+ stress and the malate exudation. Based on these data, it was concluded that the SA-related functions in Arabidopsis response to the Al3+ stress were associated with the control of oxidative stress, but not of malate exudation.
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Abbreviations
- CAT:
-
catalase
- MDA:
-
malondialdehyde
- nahG :
-
naphthalene hydroxylase G
- npr1-1 :
-
nonexpressor of pathogenesisrelative gene 1
- POD:
-
peroxidase
- ROS:
-
reactive oxygen species
- SA:
-
salicylic acid
- sid2 :
-
SA induction deficient 2
- snc1 :
-
suppressor of npr1-1, constitutive 1
- SOD:
-
superoxide dismutase
References
Aebi, H.: Catalase. — In: Bergmeyer, H.U. (ed.): Methods of Enzymatic Analysis. 3rd Ed. Pp. 273–282. Verlag-Chemie, Weinheim 1983.
Beyer, W.F., Fridovich, I.: Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. — Anal. Biochem. 161: 559–566, 1987.
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.
Cao, H., Bowling, S.A., Gordon, A.S., Dong, X.: Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. — Plant Cell 6: 1583–1592, 1994.
Delhaize, E., Ryan, P.R., Randall, P.J.: Aluminum tolerance in wheat (Triticum aextium L.). II. Aluminum-stimulated excretion of malic acid from root apices. — Plant Physiol. 103: 695–702, 1993.
Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., Ryals, J.: Requirement of salicylic acid for the induction of systemic acquired resistance. — Science 261: 754–756, 1993.
Griffith, O.W., Meister, A.: Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (s-nbutylhomocysteine sulfoximine). — J. biol. Chem. 254: 7558–7560, 1979.
Hao, L., Wang, Y., Xu, J., Feng, S.D., Ma, C.Y., Liu, C., Xu, X., Li, G.Z., Herbert, S.J.: Role of endogenous salicylic acid in Arabidopsis response to elevated SO2 exposure. — Biol. Plant. 55: 297–304, 2011.
Hao, L., Zhao, Y., Jin, D., Zhang, L., Bi, X.H., Chen, H.X., Xu, Q., Ma, C.Y., Li, G.Z.: Salicylic acid-altering Arabidopsis mutants response to salt stress. — Plant Soil 354: 81–95, 2012.
Hemeda, H.M., Klein, B.P.: Effects of naturally occurring antioxidants on peroxidase activity of vegetable extracts. — J. Food Sci. 55: 184–185, 1990.
Hoekenga, O.A., Maron, L.G., Piñeros, M.A., Cançado, G.M.A., Shaff, J., Kobayashi, Y., Ryan, P.R., Dong, B., Delhaize, E., Sasaki, T., Matsumoto, H., Yamamoto, Y., Koyama, H., Kochian, L.: AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. — Proc. nat. Acad. Sci. USA 103: 9738–9743, 2006.
Horváth, E., Pál, M., Szalai, G., Páldi, E., Janda, T.: Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. — Biol. Plant. 51: 480–487, 2007.
Jouili, H., Bouazizi, H., Ferjani, E.E.: Plant peroxidases: biomarkers of metallic stress. — Acta Physiol. Plant. 33: 2075–2082, 2011.
Jozefczak, M., Remans, T., Vangronsveld, J., Cuypers, A.: Glutathione is a key player in metal-induced oxidative stress defenses. — Int. J. mol. Sci. 13: 3145–3175, 2012.
Kang, G.Z., Li, G.Z., Liu, G.Q., Xu, W., Peng, X.Q., Wang, C.Y., Zhu, Y.J., Guo, T.C.: Exogenous salicylic acid enhances wheat drought tolerance by influence on the expression of genes related to ascorbate-glutathione cycle. — Biol. Plant. 57: 718–724, 2013.
Kinraide, T.B., Parker, D.R., Zobel, R.W.: Organic acid secretion as a mechanism of aluminium resistance: a model incorporating the root cortex, epidermis, and the external unstirred layer. — J. exp. Bot. 56: 1853–1865, 2005.
Kobayashi, Y., Kobayashi, Y., Sugimoto, M., Lakshmanan, V., Iuchi, S., Kobayashi, M., Bais, H.P., Koyama, H.: Characterization of the complex regulation of AtALMT1 expression in response to phytohormones and other inducers. — Plant Physiol. 162: 732–740, 2013.
Kochian, L.V., Hoekenga, O.A., Piňeros, M.A.: How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. — Annu. Rev. Plant Biol. 55: 459–493, 2004.
Kováčik, J., Stork, F., Klejdus, B., Grúz, J., Hedbavný, J.: Effect of metabolic regulators on aluminium uptake and toxicity in Matricaria chamomilla plants. — Plant Physiol. Biochem. 54: 140–148, 2012.
Kukavica, B.M., Veljović-Jovanović, S.D., Menckhoff, L., Lüthje, S.: Cell wall-bound cationic and anionic class III isoperoxidases of pea root: biochemical characterization and function in root growth. — J. exp. Bot. 63: 4631–4645, 2012.
Kumari, M., Taylor, G.J., Deyholos, M.K.: Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. — Mol. Genet. Genomics 279: 339–357, 2008.
Kunihiro, S., Hiramatsu, T., Kawano, T.: Involvement of salicylic acid signal transduction in aluminum-responsive oxidative burst in Arabidopsis thaliana cell suspension culture. — Plant Signal Behav. 6: 611–616, 2011.
Li, X., Clarke, J.D., Zhang, Y., Dong, X.: Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. — Mol. Plant Microbe Interact. 14: 1131–1139, 2001.
Liu, N., You, J.F., Shi, W.L., Liu, W., Yang, Z.M.: Salicylic acid involved in the process of aluminum induced citrate exudation in Glycine max L. — Plant Soil 352: 85–97, 2012.
Ma, B.H., Gao, L., Zhang, H.X., Cui, J., Shen, Z.G.: Aluminum-induced oxidative stress and changes in antioxidant defenses in the roots of rice varieties differing in Al tolerance. — Plant Cell Rep. 31: 687–696, 2012.
Ma, J.F.: Role of organic acids in detoxification of aluminumin higher plants. — Plant Cell Physiol. 41: 383–390, 2000.
Ma, J.F., Ryan, P.R., Delhaize, E.: Aluminium tolerance in plants and the complexing role of organic acids. — Trends Plant Sci. 6: 273–278, 2001.
Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.
Mukherjee, S.P., Choudhuri, M.A.: Implications of water stress induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. — Physiol. Plant. 58: 166–170, 1983.
Mutlu, S., Atici, Ö., Nalbantoğlu, 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.
Mutlu, S., Karadağoğlu, Ö., Atici, Ö., Nalbantoğlu, B.: Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. — Biol. Plant. 57: 507–513, 2013.
Pandey, P., Srivastava, R.K., Dubey, R.S.: Salicylic acid alleviates aluminum toxicity in rice seedlings better than magnesium and calcium by reducing aluminum uptake, suppressing oxidative damage and increasing antioxidative defense. — Ecotoxicology 22: 656–670, 2013.
Rivas-San Vicente, M., Plasencia, J.: Salicylic acid beyond defence: its role in plant growth and development. — J. exp. Bot. 62: 3321–3338, 2011.
Schaffer, F.Q., Buettner, G.R.: Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. — Free Radicals Biol. Med. 30: 1191–1212, 2001.
Shalata, A., Tal, M.: The effect of salt stress on lipid peroxidation and antioxidants in the leaf of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. — Physiol. Plant. 104: 167–174, 1998.
Tamás, L., Huttová, J., Mistrík, I.: Effect of aluminum on peroxidase activity in roots of Al-sensitive and Al-resistant barley cultivars. — Rost. Výroba 48: 76–79, 2002.
Tao, S.Y., Sun, L.H., Ma, C.Y., Li, L.L., Li, G.Z., Hao, L.: Reducing basal salicylic acid enhances Arabidopsis tolerance to lead or cadmium. — Plant Soil 372: 309–318, 2013.
Wildermuth, M.C., Dewdney, J., Wu, G., Ausubel, F.M.: Isochorismate synthase is required to synthesize salicylic acid for plant defence. — Nature 414: 562–565, 2001.
Yang, L.T., Qi, Y.P., Jiang, H.X., Chen, L.S.: Roles of organic acid anion secretion in aluminium tolerance of higher plants. — BioMed Res. Int. 2013, Article ID 173682.
Zawoznik, M.S., Groppa, M.D., Tomaro, M.L., Benavides, M.P.: Endogenous salicylic acid potentiates cadmiuminduced oxidative stress in Arabidopsis thaliana. — Plant Sci. 173: 190–197, 2007.
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Acknowledgements: This research was supported by the National Natural Science Foundation of China (Grant No. 31270446, 30570445), and the Natural Science Foundation of Liaoning Province (No. 2013020145). D.Y. Guo and S.Y. Zhao contributed equally to this work.
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Guo, D.Y., Zhao, S.Y., Huang, L.L. et al. Aluminum tolerance in Arabidopsis thaliana as affected by endogenous salicylic acid. Biol Plant 58, 725–732 (2014). https://doi.org/10.1007/s10535-014-0439-0
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DOI: https://doi.org/10.1007/s10535-014-0439-0