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Overexpression of Arabidopsis dehydration-responsive element-binding protein 2C confers tolerance to oxidative stress

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Molecules and Cells

Abstract

Dehydration-responsive element-binding proteins (DREBs) regulate plant responses to environmental stresses. In the current study, transcription of DREB2C, a class 2 Arabidopsis DREB, was induced by a superoxide anion propagator, methyl viologen (MV). The oxidative stress tolerance of DREB2C-overexpressing transgenic plants was significantly greater than that of wild-type plants, as measured by ion leakage and chlorophyll fluorescence under light conditions. The transcriptional activity of several ascorbate peroxidase (APX) genes as well as APX protein activity was induced in DREB2C overexpressors. Additionally, the level of H2O2 in the overexpressors was lower than in wt plants under similar oxidative stress conditions. An electrophoretic mobility shift assay and transient activatorreporter assay showed that APX2 expression was regulated by heat shock factor A3 (HsfA3) and that HsfA3 is regulated at the transcriptional level by DREB2C. These results suggest that DREB2C plays an important role in promoting oxidative stress tolerance in Arabidopsis.

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References

  • Agarwal, P., Agarwal, P.K., Nair, S., Sopory, S.K., and Reddy, M.K. (2007). Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. Mol. Genet. Genomics 277, 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Almoguera, C., Prieto-Dapena, P., Díaz-Martín, J., Espinosa, J.M., Carranco, R., and Jordano, J. (2009). The HaDREB2 transcription factor enhances basal thermotolerance and longevity of seeds through functional interaction with HaHSFA9. BMC Plant Biol. 9, 75.

    Article  PubMed  Google Scholar 

  • Bailey, T.L., and Elkan, C. (1995). The value of prior knowledge in discovering motifs with MEME. In Proceedings of the 3rd International Conference on Intelligent Systems for Molecular Biology, (AAAI Press, Menlo Park), pp. 21–29.

    Google Scholar 

  • Baker, N.R., and Rosenqvist, E. (2004). Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J. Exp. Bot. 55, 1607–1621.

    Article  PubMed  CAS  Google Scholar 

  • Chen, H., Hwang, J.E., Lim, C.J., Kim, D.Y., Lee, S.Y., and Lim, C.O. (2010). Arabidopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem. Biophys. Res. Commun. 401, 238–244.

    Article  PubMed  CAS  Google Scholar 

  • Giacomelli, L., Masi, A., Ripoll, D.R., Lee, M.J., and van Wijk, K.J. (2007). Arabidopsis thaliana deficient in two chloroplast ascorbate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low. Plant Mol. Biol. 65, 627–644.

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., and Thomashow, M.F. (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104–106.

    Article  PubMed  CAS  Google Scholar 

  • Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P. (1999). Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657.

    Article  PubMed  CAS  Google Scholar 

  • Kim, H.S., Park, B.O., Yoo, J.H., Jung, M.S., Lee, S.M., Han, H.J., Kim, K.E., Kim, S.H., Lim, C.O., Yun, D.J., et al. (2007). Identification of a calmodulin-binding NAC protein as a transcriptional repressor in Arabidopsis. J. Biol. Chem. 282, 36292–36302.

    Article  PubMed  CAS  Google Scholar 

  • Lee, K., Han, K.S., Kwon, Y.S., Lee, J.H., Kim, S.H., Chung, W.S., Kim, Y., Chun, S.-S., Kim, H.K., and Bae, D.-W. (2009). Identification of potential DREB2C targets in Arabidopsis thaliana plants overexpressing DREB2C using proteomic analysis. Mol. Cells 28, 383–388.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S.-J., Kang, J.-Y., Park, H.-J., Kim, M.D., Bae, M.S., Choi, H.-I., and Kim, S.Y. (2010). DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol. 153, 716–727.

    Article  PubMed  CAS  Google Scholar 

  • Lim, C.J., Hwang, J.E., Chen, H., Hong, J.K., Yang, K.A., Choi, M.S., Lee, K.O., Chung, W.S., Lee, S.Y., and Lim, C.O. (2007). Over-expression of the Arabidopsis DRE/CRT-binding transcription factor DREB2C enhances thermotolerance. Biochem. Biophys. Res. Commun. 362, 431–436.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406.

    Article  PubMed  CAS  Google Scholar 

  • Matsukura, S., Mizoi, J., Yoshida, T., Todaka, D., Ito, Y., Maruyama, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2010). Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stress-responsive genes. Mol. Genet. Genomics 283, 185–196.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., and Breusegem, F.V. (2004). Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490–498.

    Article  PubMed  CAS  Google Scholar 

  • Noriega, G.O., Yannarelli, G.G., Balestrasse, K.B., Batlle, A., and Tomaro, M.L. (2007). The effect of nitric oxide on heme oxygenase gene expression in soybean leaves. Planta 226, 1155–1163.

    Article  PubMed  CAS  Google Scholar 

  • Oh, S.J., Kwon, C.W., Choi, D.W., Song, S.I., and Kim, J.K. (2007). Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol. J. 5, 646–656.

    Article  PubMed  CAS  Google Scholar 

  • Panchuk, I.I., Volkov, R.A., and Schöffl, F. (2002). Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol. 129, 838–853.

    Article  PubMed  CAS  Google Scholar 

  • Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem. Biophys. Res. Commun. 290, 998–1009.

    Article  PubMed  CAS  Google Scholar 

  • Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006). Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. USA 103, 18822–18827.

    Article  PubMed  CAS  Google Scholar 

  • Scarpeci, T.E., Zanor, M.I., Carrillo, N., Mueller-Roeber, B., and Valle, E.M. (2008). Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol. Biol. 66, 361–378.

    Article  PubMed  CAS  Google Scholar 

  • Schramm, F., Larkindale, J., Kiehlmann, E., Ganguli, A., Englich, G., Vierling, E., and von Koskull-Döring, P. (2008). A cascade of transcription factor DREB2A and heat stress transcription factor HsfA3 regulates the heat stress response of Arabidopsis. Plant J. 53, 264–274.

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z., Wei, Y., and Collinge, D.B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187–1194.

    Article  CAS  Google Scholar 

  • Xing, Y., Jia, W., and Zhang, J. (2007). AtMEK1 mediates stress-induced gene expression of CAT1 catalase by triggering H2O2 production in Arabidopsis. J. Exp. Bot. 58, 2969–2981.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994). A novel cisacting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251–264.

    Article  PubMed  CAS  Google Scholar 

  • Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida, T., Sakuma, Y., Todaka, D., Maruyama, K., Qin, F., Mizoi, J., Kidokoro, S., Fujita, Y., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2008). Functional analysis of an Arabidopsis heat-shock transcription factor HsfA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system. Biochem. Biophys. Res. Commun. 368, 515–521.

    Article  PubMed  CAS  Google Scholar 

  • Yu, B., Xu, C., and Benning, C. (2002). Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc. Natl. Acad. Sci. USA 99, 5732–5737.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Chae Oh Lim.

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Hwang, J.E., Lim, C.J., Chen, H. et al. Overexpression of Arabidopsis dehydration-responsive element-binding protein 2C confers tolerance to oxidative stress. Mol Cells 33, 135–140 (2012). https://doi.org/10.1007/s10059-012-2188-2

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  • DOI: https://doi.org/10.1007/s10059-012-2188-2

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