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CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis

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Abstract

C-repeat/dehydration-responsive element binding factors (CBFs) can induce the expression of a suite of cold-responsive genes to increase plant cold tolerance, and inducer of CBF expression 1 (ICE1) is a major activator for CBF. In the present study, we isolated the full-length cDNAs of ICE1 and CBF from Camellia sinensis, designated as CsICE1 and CsCBF1, respectively. The deduced protein CsICE1 contains a highly conserved basic helix-loop-helix (bHLH) domain and C-terminal region of ICE1-like proteins. CsCBF1 contains all conserved domains of CBFs in other plant species and can specifically bind to the C-repeat/dehydration-responsive element (CRT/DRE) as confirmed by electrophoretic mobility shift assay. The transcription of CsICE1 had no apparent alteration after chilling treatment (4°C). CsCBF1 expression was not detected in normal temperature (20°C) but was induced immediately and significantly by low temperature (4°C). Our results suggest that ICE1–CBF cold-response pathway is conserved in tea plants. CsICE1 and CsCBF1, two components of this pathway, play roles in cold responses in tea plants.

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References

  • Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  PubMed  CAS  Google Scholar 

  • Badawi M, Reddy YV, Agharbaoui Z, Tominaga Y, Danyluk J, Sarhan F, Houde M (2008) Structure and functional analysis of wheat ICE (inducer of CBF expression) genes. Plant Cell Physiol 49:1237–1249

    Article  PubMed  CAS  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (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

    Article  PubMed  CAS  Google Scholar 

  • Benedict C, Geisler M, Trygg J, Huner N, Hurry V (2006a) Consensus by Democracy. Using meta-analyses of microarray and genomic data to model the cold acclimation signaling pathway in Arabidopsis. Plant Physiol 141:1219–1232

    Article  PubMed  CAS  Google Scholar 

  • Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner N, Finn CE, Chen THH, Hurry V (2006b) The CBF1-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 29:1259–1272

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Gene Dev 17:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55

    Article  PubMed  CAS  Google Scholar 

  • El Kayal W, Navarro M, Marque G, Keller G, Marque C, Teulieres C (2006) Expression profile of CBF-like transcriptional factor genes from Eucalyptus in response to cold. J Exp Bot 57:2455–2469

    Article  PubMed  CAS  Google Scholar 

  • Fursova OV, Pogorelko GV, Tarasov VA (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429:98–103

    Article  PubMed  CAS  Google Scholar 

  • Gao SQ, Chen M, Xia LQ, Xiu HJ, Xu ZS, Li LC, Zhao CP, Cheng XG, Ma YZ (2009) A cotton (Gossypium hirsutum) DRE-binding transcription factor gene, GhDREB, confers enhanced tolerance to drought, high salt, and freezing stresses in transgenic wheat. Plant Cell Rep 28:301–311

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (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

    Article  PubMed  CAS  Google Scholar 

  • 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 127:910–917

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Iu B, 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

    Article  PubMed  CAS  Google Scholar 

  • Jing D, Agnew J, Patton WF, Hendrickson J, Beechem JM (2003) A sensitive two-color electrophoretic mobility shift assay for detecting both nucleic acids and protein in gels. Proteomics 3:1172–1180

    Article  PubMed  CAS  Google Scholar 

  • Kitashiba H, Ishizaka T, Isuzugawa K, Nishimura K, Suzuki T (2004) Expression of a sweet cherry DREB1/CBF ortholog in Arabidopsis confers salt and freezing tolerance. J Plant Physiol 161:1171–1176

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  PubMed  CAS  Google Scholar 

  • Li F, Guo SY, Zhao YA, Chen DZ, Chong K, Xu YY (2010a) Overexpression of a homopeptide repeat-containing bHLH protein gene (OrbHLH001) from Dongxiang Wild Rice confers freezing and salt tolerance in transgenic Arabidopsis. Plant Cell Rep 29:977–986

    Article  PubMed  CAS  Google Scholar 

  • Li XW, Feng ZG, Yang HM, Zhu XP, Liu J, Yuan HY (2010b) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt- and dehydration-tolerance in tobacco. Biochem Biophys Res Commun 394:354–359

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed  CAS  Google Scholar 

  • Pires N, Dolan L (2010) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27:862–874

    Article  PubMed  CAS  Google Scholar 

  • Puhakainen T, Li C, Boije-Malm M, Kangasjarvi J, Heino P, Palva ET (2004) Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol 136:4299–4307

    Article  PubMed  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, 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

    Article  PubMed  CAS  Google Scholar 

  • Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, 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

    Article  PubMed  CAS  Google Scholar 

  • 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 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599

    Article  CAS  Google Scholar 

  • Wang L, Li XW, Zhao Q, Jing SL, Chen SF, Yuan HY (2009) Identification of genes induced in response to low-temperature treatment in tea leaves. Plant Mol Biol Rep 27:257–265

    Article  CAS  Google Scholar 

  • Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plantarum 127:167–181

    Article  CAS  Google Scholar 

  • Welling A, Palva ET (2008) Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol 147:1199–1211

    Article  PubMed  CAS  Google Scholar 

  • 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 6:251–264

    Article  PubMed  CAS  Google Scholar 

  • Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (Inducer of CBF expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133:910–918

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Fowler SG, Cheng HM, Lou YG, Rhee SY, Stockinger EJ, Thomashow MF (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

    Article  PubMed  CAS  Google Scholar 

  • Zhao TJ, Sun S, Liu Y, Liu JM, Liu Q, Yan YB, Zhou HM (2006) Regulating the drought-responsive element (DRE)-mediated signaling pathway by synergic functions of trans-active and trans-inactive DRE binding factors in Brassica napus. J Biol Chem 281:10752–10759

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Professor Shu Wei for critical comments and language editing on the manuscript. This work was supported by the National Natural Science Foundation of China (No. 30871568), the National Key Technology R&D Program for the 12th Five year Plan of China (No. 2011BAD01B01), the Specialized Research Fund for the Doctoral Program of Higher Education of China (No. 20103418110001) and the Natural Science Foundation of Auhui province (No. 090411014).

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Authors and Affiliations

  1. Key Laboratory of Tea Biochemistry and Biotechnology, Ministry of Education and Ministry of Agriculture, Anhui Agriculture University, Hefei, 230036, China

    Yu Wang, Chang-Jun Jiang, Ye-Yun Li, Chao-Ling Wei & Wei-Wei Deng

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  1. Yu Wang
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  2. Chang-Jun Jiang
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  3. Ye-Yun Li
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  4. Chao-Ling Wei
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Correspondence to Chang-Jun Jiang.

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Communicated by H. Judelson.

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Wang, Y., Jiang, CJ., Li, YY. et al. CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis . Plant Cell Rep 31, 27–34 (2012). https://doi.org/10.1007/s00299-011-1136-5

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