Abstract
Plant productivity is greatly affected by environmental stresses such as drought, salt, and freezing. We previously described a C-repeat binding transcription factor from maize (ZmCBF3) that was upregulated by both abscisic acid and low-temperature and actively expressed during embryogenesis. To understand the stress response in rice, transgenic ZmCBF3 rice with ubiquitin promoter was developed. T3 generation was planted and analyzed. The results showed that overexpression of ZmCBF3 in rice did not cause growth retardation under normal growth conditions with improved tolerance to drought, high-salt, and low-temperature stresses. Moreover, the transgenic rice grain yield was similar to wild type plants under normal conditions. The transgenic plants showed enhanced survival rate and reduced malondialdehyde content and relative conductivity under drought, salt, and low-temperature stresses. ZmCBF3 overexpression in transgenic rice increased the transcript levels of stress-induced genes and enhanced the tolerance to drought, salt, and low-temperature stresses.
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References
Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27(3):411–424. doi:10.1007/s00299-007-0474-9
Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129(4):1781–1787. doi:10.1104/pp.003046
Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18(4):675–689
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, 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(4):751–763
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690
Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137(3):961–968. doi:10.1104/pp.104.058354
Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49(5):459–471
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124(4):1854–1865
Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130(2):639–648. doi:10.1104/pp.006478
Hiei Y, Komari T (2008) Agrobacterium-mediated transformation of rice using immature embryos or calli induced from mature seed. Nat Protoc 3(5):824–834. doi:10.1038/nprot.2008.46
Hsieh TH, Lee JT, Charng YY, Chan MT (2002) Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol 130(2):618–626. doi:10.1104/pp.006783
Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, 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(1):141–153. doi:10.1093/pcp/pci230
Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127(3):910–917
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280(5360):104–106
Jung C, Seo JS, Han SW, Koo YJ, Kim CH, Song SI, Nahm BH, Choi YD, Cheong JJ (2008) Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol 146(2):623–635. doi:10.1104/pp.107.110981
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17(3):287–291. doi:10.1038/7036
Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45(3):346–350
Kizis D, Pages M (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 30(6):679–689
Knight H, Zarka DG, Okamoto H, Thomashow MF, Knight MR (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol 135(3):1710–1717. doi:10.1104/pp.104.043562
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, 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(8):1391–1406
Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229(3):605–615. doi:10.1007/s00425-008-0857-3
Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, 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
Miller A, Galiba G, Dubcovsky J (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-Am2 in Triticum monococcum. Mol Gen Genomics 275(2):193–203. doi:10.1007/s00438-005-0076-6
Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351
Oh SJ, Kwon CW, Choi DW, Song SI, Kim JK (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J 5(5):646–656. doi:10.1111/j.1467-7652.2007.00272.x
Pellegrineschi A, Reynolds M, Pacheco M, Brito RM, Almeraya R, Yamaguchi-Shinozaki K, Hoisington D (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47(3):493–500. doi:10.1139/g03-140
Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45(8):1042–1052. doi:10.1093/pcp/pch118
Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59(4):533–551. doi:10.1007/s11103-005-2498-2
Stockinger EJ, Gilmour SJ, Thomashow MF (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 USA 94(3):1035–1040
Tang Qy(2010) DPS data processing system—experimental design, statistical analysis and data mining, 2nd edn. Science Press, Beijing
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16(9):2481–2498. doi:10.1105/tpc.104.022699
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97(21):11632–11637. doi:10.1073/pnas.190309197
Wang X, Liu L, Liu S, Sun X, Deng Z, Pi Y, Tang K (2004) Isolation and molecular characterization of a new CRT binding factor gene from Capsella bursa-pastoris. J Biochem Mol Biol 37(5):538–545
Wang L, Luo Y, Zhang L, Zhao J, Hu Z, Fan Y, Zhang C (2008) Isolation and characterization of a C-repeat binding transcription factor from maize. J Integr Plant Biol 50(8):965–974. doi:10.1111/j.1744-7909.2008.00683.x
Xiao BZ, Chen X, Xiang CB, Tang N, Zhang QF, Xiong LZ (2009) Evaluation of seven function-known candidate genes for their effects on improving drought resistance of transgenic rice under field conditions. Mol Plant 2(1):73–83
Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(90001):S165–S183. doi:10.1105/tpc.000596
Xue GP (2002) An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a) (C/t)CGAC motif. Biochim Biophys Acta 1577(1):63–72. doi:S0167478102004104
Xue GP (2003) The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J 33(2):373–383. doi:10.1046/j.1365-313X.2003.01630.x
Yamaguchi-Shinozaki K, 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(2):251–264. doi:10.1105/tpc.6.2.251
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. doi:10.1146/annurev.arplant.57.032905.105444
Zhang ZL, Huang X, Chen YF (2008) Plant physiology worksheets. Higher Education Press, Beijing
Acknowledgments
This work was supported by the National Key Basic Research Program (Grant Numbers 2010CB125903 and 2007CB108801) and the National Special Program for Genetically Modified Organisms Development (Grant Number 2009ZX08009-16B).
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Xu, M., Li, L., Fan, Y. et al. ZmCBF3 overexpression improves tolerance to abiotic stress in transgenic rice (Oryza sativa) without yield penalty. Plant Cell Rep 30, 1949–1957 (2011). https://doi.org/10.1007/s00299-011-1103-1
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DOI: https://doi.org/10.1007/s00299-011-1103-1