Differential Regulatory Mechanisms of CBF Regulon Between Nipponbare (Japonica) and 93-11 (Indica) During Cold Acclimation

doi:10.1016/S1672-6308(13)60121-3

Abstract

Abstract:

Nine CBF/DREB1 homologous genes in rice were obtained by BLAST search in the NCBI database, which share conserved amino acid sequences with DREB1 protein in Arabidopsis. Three CBF genes organized in tandem, named OsCBF1, OsCBF2 and OsCBF3, showed a transient induction in the process of cold acclimation, much stronger in indica rice 93-11 compared with japonica rice Nipponbare. The candidate downstream genes OsLIP5 and OsLIP9 were induced in 93-11 but not in Nipponbare. The differential expression of CBF regulon might be caused by polymorphisms within promoter sequences between these two rice varieties. These results could be useful for utilization of CBF/DREB1 genes and illustration of differences in chilling tolerance between indica and japonica rice varieties.

Key words: rice, CBF/DREB1, cold acclimation, gene expression, promoter analysis

PAN Xiao-wu, LI Yong-chao, LI Xiao-xiang, LIU Wen-qiang, MING Jun, LU Ting-ting, TAN Jiang, SHENG Xin-nian. Differential Regulatory Mechanisms of CBF Regulon Between Nipponbare (Japonica) and 93-11 (Indica) During Cold Acclimation[J]. RICE SCIENCE, 2013, 20(3): 165-172.

References

Canella D, Gilmour S J, Kuhn L A, Thomashow M F. 2010. DNA binding by the Arabidopsis CBF1 transcription factor requires the PKKP/RAGRxKFxETRHP signature sequence. Biochim Biophys Acta, 1799: 454–462.
Carvallo M A, Pino M T, Jekni? Z, Zou C, Doherty C J, Shiu S H, Chen T H H, Thomashow M F. 2011. A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot, 62(11): 3807–3819.
Chinnusamy V, Ohta M, Kanrar S, Lee B H, Hong X, Agarwal M, Zhu J K. 2003. ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev, 17: 1043–1054.
Dubouzet J G, Sakuma Y, Ito Y, Kasuga M, Dubouzet E G, 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: 751–763.
Fowler S, Thomashow M F. 2002. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell Online, 14: 1675–1690.
Hannah M A, Wiese D, Freund S, Fiehn O, Heyer a G, Hincha D K. 2006. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol, 142: 98–112.
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: 141–153.
Jaglo K R, Kleff S, Amundsen K L, Zhang X, Haake V, Zhang J Z, Deits T, Thomashow M F. 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: 910–917.
Kato-Noguchi H. 2008. Low temperature acclimation mediated by ethanol production is essential for chilling tolerance in rice roots. Plant Signal Behav, 3: 202–203.
Kuk Y I, Shin J S, Burgos N R, Hwang T E, Han O, Cho B H, Jung S, Guh J O. 2003. Antioxidative enzymes offer protection from chilling damage in rice plants. Crop Sci, 43: 2109–2117.
Kume S, Kobayashi F, Ishibashi M, Ohno R, Nakamura C, Takumi S. 2005. Differential and coordinated expression of Cbf and Cor/Lea genes during long-term cold acclimation in two wheat cultivars showing distinct levels of freezing tolerance. Genes Genet Syst, 80: 185–197.
Lee B H, Henderson D A, Zhu J K. 2005. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell, 17: 3155–3175.
Li X, Dai C C, Jiao D M, Foyer C H. 2006. Effects of low temperature in the light on antioxidant contents in rice (Oryza sativa L.) indica and japonica subspecies seedlings. J Plant Physiol Mol Biol, 32: 345–353. (in Chinese with English abstract)
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: 1391–1406.
Liu F X, Xu W Y, Wei Q, Zhang Z H, Xing Z, Tan L B, Di C, Yao D X, Wang C C, Tan Y J, Yan H, Ling Y, Sun C Q, Xue Y B, Su Z. 2010. Gene expression profiles deciphering rice phenotypic variation between Nipponbare (japonica) and 93-11 (indica) during oxidative stress. PLoS One, 5: e8632.
Mckhann H I, Gery C, Berard A, Leveque S, Zuther E, Hincha D K, de Mita S, Brunel D, Teoule E. 2008. Natural variation in CBF gene sequence, gene expression and freezing tolerance in the Versailles core collection of Arabidopsis thaliana. BMC Plant Biol, 8: 105.
Miura K, Jin J B, Lee J, Yoo C Y, Stirm V, Miura T, Ashworth E N, Bressan R A, Yun D J, Hasegawa P M. 2007. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell, 19: 1403–1414.
Novillo F, Alonso J M, Ecker J R, 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 USA, 101: 3985–3990.
Novillo F, Medina J, Salinas J. 2007. Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA, 104: 21002–21007.
Pennycooke J C, Cheng H, Stockinger E J. 2008. Comparative genomic sequence and expression analyses of Medicago truncatula and alfalfa subspecies falcata COLD-ACCLIMATION-SPECIFIC genes. Plant Physiol, 146: 1242–1254.
Sakuma Y, Liu Q, Dubouzet J G, Abe H, Shinozaki K, 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.
Thomashow M F. 1999. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol, 50: 571–599.
Thomashow M F. 2010. Molecular basis of plant cold acclimation: Insights gained from studying the CBF cold response pathway. Plant Physiol, 154: 571–577.
Tian Y, Zhang H W, Pan X W, Chen X L, Zhang Z J, Lu X Y, Huang R F. 2011. Overexpression of ethylene response factor TERF2 confers cold tolerance in rice seedlings. Transgenic Res, 20: 857–866.
Wang Y, Hua J. 2009. A moderate decrease in temperature induces COR15a expression through the CBF signaling cascade and enhances freezing tolerance. Plant J, 60: 340–349.
Yan S P, Zhang Q Y, Tang Z C, Su W A, Sun W N. 2006. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Prot, 5: 484–496.
Yu X, Peng Y H, Zhang M H, Shao Y J, Su W A, Tang Z C. 2006. Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res, 16: 599–608.
Yun K Y, Park M R, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic V B, Bruskiewich R, de los Reyes B G. 2010. Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol, 10(1): 16.
Zhang X, Fowler S G, Cheng H, Lou Y, Rhee S Y, Stockinger E J, Thomashow M F. 2004. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J, 39: 905–919.
Zhu J, Dong C H, Zhu J K. 2007. Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol, 10: 290–295.

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