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Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis

  • Zhang, Yang (College of Bioscience and Biotechnology, Yangzhou University) ;
  • Chen, Chen (College of Bioscience and Biotechnology, Yangzhou University) ;
  • Jin, Xiao-Fen (Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences) ;
  • Xiong, Ai-Sheng (Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences) ;
  • Peng, Ri-He (Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences) ;
  • Hong, Yi-Huan (College of Bioscience and Biotechnology, Yangzhou University) ;
  • Yao, Quan-Hong (Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences) ;
  • Chen, Jian-Min (College of Bioscience and Biotechnology, Yangzhou University)
  • Published : 2009.08.31
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Abstract

OsDREB1D, a special DREB (dehydration responsive element binding protein) homologous gene, whose transcripts cannot be detected in rice (Oryza sativa L), either with or without stress treatments, was amplified from the rice genome DNA. The yeast one-hybrid assay revealed that OsDREB1D was able to form a complex with the dehydration responsive element/C-repeat motif. It can also bind with a sequence of LTRE (low temperature responsive element). To analyze the function of OsDREB1D, the gene was transformed and over-expressed in Arabidopsis thaliana cv. Columbia. Results indicated that the over-expression of OsDREB1D conferred cold and high-salt tolerance in transgenic plants, and that transgenic plants were also insensitive to ABA (abscisic acid). From these data, we deduced that this OsDREB1D gene functions similarly as other DREB transcription factors. The expression of OsDREB1D in rice may be controlled by a special mechanism for the redundancy of function.

Keywords

References

  1. Yamaguchi-Shinozaki, K. and Shinozaki, K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251-264 https://doi.org/10.1105/tpc.6.2.251
  2. Gamboa, M. C., Rasmussen-Poblete, S., Valenzuela, P. D. and Krauskopf, E. (2007) Isolation and characterization of a cDNA encoding a CBF transcription factor from E. globulus. Plant Physiol. Biochem. 45, 1-5 https://doi.org/10.1016/j.plaphy.2006.12.006
  3. Kim, Y. H., Yang, K. S., Ryu, S. H., Kim, K. Y., Song, W. K., Kwon, S. Y., Lee, H. S., Bang, J. W. and Kwak, S. S. (2008) Molecular characterization of a cDNA encoding DRE-binding transcription factor from dehydration-treated fibrous roots of sweetpotato. Plant. Physiol. Biochem. 46, 196-204 https://doi.org/10.1016/j.plaphy.2007.09.012
  4. Tang, M., Lu, S., Jing, Y., Zhou, X., Sun, J. and Shen, S. (2005) Isolation and identification of a cold-inducible gene encoding a putative DRE-binding transcription factor from Festuca arundinacea. Plant. Physiol. Biochem. 43, 233-239 https://doi.org/10.1016/j.plaphy.2005.01.015
  5. 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 https://doi.org/10.1126/science.280.5360.104
  6. Gilmour, S. J., Sebolt, A. M., Salazar, M. P., Everard, J. D. and Thomashow, M. F. (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant. Physiol. 124, 1854-1865 https://doi.org/10.1104/pp.124.4.1854
  7. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17, 287-291 https://doi.org/10.1038/7036
  8. 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 https://doi.org/10.1105/tpc.10.8.1391
  9. Novillo, F., Alonso, J. M., Ecker, J. R. and Salinas, J. (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 101, 3985-3990 https://doi.org/10.1073/pnas.0303029101
  10. Haake, V., Cook, D., Riechmann, J. L., Pineda, O., Thomashow, M. F. and Zhang, J. Z. (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant. Physiol. 130, 639-648 https://doi.org/10.1104/pp.006478
  11. Dubouzet, J. G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E. G., Miura, S., Seki, M., Shinozaki, K. and Yamaguchi- Shinozaki, K. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant. J. 33, 751-763 https://doi.org/10.1046/j.1365-313X.2003.01661.x
  12. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant. Cell Physiol. 47, 141-153 https://doi.org/10.1093/pcp/pci230
  13. Baker, S. S., Wilhelm, K. S. and Thomashow, M. F. (1994) The 5'-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant. Mol. Biol. 24, 701-713 https://doi.org/10.1007/BF00029852
  14. Jiang, C., Iu, B. and Singh, J. (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. Plant. Mol. Biol. 30, 679-684 https://doi.org/10.1007/BF00049344
  15. Gilmour, S. J., Zarka, D. G., Stockinger, E. J., Salazar, M. P., Houghton, J. M. and Thomashow, M. F. (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant. J. 16, 433-442 https://doi.org/10.1046/j.1365-313x.1998.00310.x
  16. Kobayashi, F., Takumi, S. and Nakamura, C. (2008) Increased freezing tolerance in an ABA-hypersensitive mutant of common wheat. J. Plant. Physiol. 165, 224-232 https://doi.org/10.1016/j.jplph.2006.11.004
  17. Kurkela, S. and Borg-Franck, M. (1992) Structure and expression of kin2, one of two cold- and ABA-induced genes of Arabidopsis thaliana. Plant. Mol. Biol. 19, 689-692 https://doi.org/10.1007/BF00026794
  18. Stockinger, E. J., Gilmour, S. J. and Thomashow, M. F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/ DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl. Acad. Sci. U.S.A. 94, 1035-1040 https://doi.org/10.1073/pnas.94.3.1035
  19. Maruyama, K., Sakuma, Y., Kasuga, M., Ito, Y., Seki, M., Goda, H., Shimada, Y., Yoshida, S., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/ CBF3 transcriptional factor using two microarray systems. Plant. J. 38, 982-993 https://doi.org/10.1111/j.1365-313X.2004.02100.x
  20. Shinozaki, K., Yamaguchi-Shinozaki, K. and Seki, M. (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr. Opin. Plant. Biol. 6, 410-417 https://doi.org/10.1016/S1369-5266(03)00092-X
  21. Zhu, J. K. (2002) Salt and drought stress signal transduction in plants. Annu. Rev. Plant. Biol. 53, 247-273 https://doi.org/10.1146/annurev.arplant.53.091401.143329
  22. Medina, J., Bargues, M., Terol, J., Perez-Alonso, M. and Salinas, J. (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression Is regulated by low temperature but not by abscisic acid or dehydration. Plant. Physiol. 119, 463-470 https://doi.org/10.1104/pp.119.2.463
  23. Nakashima, K., Shinwari, Z. K., Sakuma, Y., Seki, M., Miura, S., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant. Mol. Biol. 42, 657-665 https://doi.org/10.1023/A:1006321900483
  24. Shinwari, Z. K., Nakashima, K., Miura, S., Kasuga, M., Seki, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem. Biophys. Res. Commun. 250, 161-170 https://doi.org/10.1006/bbrc.1998.9267
  25. Chen, M., Wang, Q. Y., Cheng, X. G., Xu, Z. S., Li, L. C., Ye, X. G., Xia, L. Q. and Ma, Y. Z. (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem. Biophys. Res. Commun. 353, 299-305 https://doi.org/10.1016/j.bbrc.2006.12.027
  26. Chan, S. W., Henderson, I. R. and Jacobsen, S. E. (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat. Rev. Genet 6, 351-360 https://doi.org/10.1038/nrg1601
  27. Bender, J. and Fink, G. R. (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83, 725-734 https://doi.org/10.1016/0092-8674(95)90185-X
  28. Zhang, X., Henriques, R. and Lin, S. S. (2006) Agrobacteriummediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641-646 https://doi.org/10.1038/nprot.2006.97
  29. Peng, R. H., Huang, X. M., Li, X., Sun, A. J., Yao, Q. H. and Peng, Y. L. (2001) Construction of a plant binary expression vector containing intro-kanamycin gene and transformation in nicotiana tabacum. Acta. Phytophysiologica. Sinica. 27, 55-60
  30. Mitsuhara, I., Ugaki, M., Hirochika, H., Ohshima, M., Murakami, T., Gotoh, Y., Katayose, Y., Nakamura, S., Honkura, R., Nishimiya, S., Ueno, K., Mochizuki, A., Tanimoto, H., Tsugawa, H., Otsuki, Y. and Ohashi, Y. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant. Cell. Physiol. 37, 49-59 https://doi.org/10.1093/oxfordjournals.pcp.a028913
  31. Gallie, D. R., Sleat, D. E., Watts, J., Turner, P. C. and Wilson, T. M. A. (1987) A comparison of eukaryotic viral 50-leader sequences as enhancers of mRNA expression in vivo. Nucl. Acids. Res. 15, 8693-8711 https://doi.org/10.1093/nar/15.21.8693
  32. Xiong, L., Lee, B., Ishitani, M., Lee, H., Zhang, C. and Zhu, J. K. (2001) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev. 15, 1971-1984 https://doi.org/10.1101/gad.891901
  33. Zhu, B., Xiong, A. S., Peng, R. H., Xu, J., Zhou, J., Xu, J. T., Jin, X. F., Zhang, Y., Hou, X. L. and Yao, Q. H. (2008) Heat stress protection in Aspen sp1 transgenic Arabidopsis thaliana. BMB Rep. 41, 382-387
  34. Qin, Q. L., Liu, J. G., Zhang, Z., Peng, R. H., Xiong, A. S., Yao, Q. H. and Chen, J. M. (2007) Isolation, optimization, and functional analysis of the cDNA encoding transcription factor OsDREB1B in Oryza Sativa L. Mol. Breeding 19, 329-340 https://doi.org/10.1007/s11032-006-9065-7
  35. Gietz, R. D. and Woods, R. A. (2006) Yeast transformation by the LiAc/SS Carrier DNA/PEG method. Methods Mol. Biol. 313, 107-120

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