Skip to main content
Log in

Overexpression of a Camellia sinensis DREB transcription factor gene (CsDREB) increases salt and drought tolerance in transgenic Arabidopsis thaliana

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Dehydration-responsive element-binding protein (DREB) transcription factors play key roles in plant stress signal transduction pathways. We herein describe the functions of a Camellia sinensis DREB transcription factor (CsDREB) in response to abiotic stress. Subcellular localization analyses indicated that the CsDREB localizes to the nucleus. CsDREB expression in C. sinensis leaves was induced by heat, cold, drought, high salinity, H2O2, and exogenous abscisic acid (ABA). Additionally, CsDREB showed no transcriptional activation in Saccharomyces cerevisiae. Transgenic Arabidopsis thaliana plants overexpressing CsDREB exhibited enhanced tolerance to salt and drought stresses. The overexpression of CsDREB in A. thaliana plants resulted in the up-regulated expression of ABA-dependent stress-induced genes (i.e., AtRD29B, AtRAB18, AtABI1, and AtABI2) and ABAindependent stress-induced genes (i.e., AtCOR15a and AtRD29A). Furthermore, an analysis of the CsDREB promoter sequence revealed the presence of several abiotic and biotic stress-related motifs, along with the developmental stageand tissue-specific elements. An examination of the transient expression of the CsDREB promoter in Nicotiana benthamiana leaves revealed that the promoter is highly responsive to ABA and methyl jasmonate. Collectively, these results suggest that CsDREB may increase plant tolerance to salt and drought stresses via both ABA-dependent and ABAindependent pathways.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plantarum 54:201–212

    Article  CAS  Google Scholar 

  • Ba ANN, Pogoutse A, Provart N, Moses AM (2009) NLStradamus: a simple hidden markov model for nuclear localization signal prediction. BMC Bioinformatics 10:202

    Article  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39:205–207

    Article  CAS  Google Scholar 

  • Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305

    Article  CAS  PubMed  Google Scholar 

  • Chen PY, Wang CK, Soong SC, To KY (2003) Complete sequence of the binary vector pBI121 and its application in cloning T-DNA insertion from transgenic plants. Mol Breeding 11:287–293

    Article  CAS  Google Scholar 

  • Das A, Mukhopadhyai M, Sarkar B, Saha D, Mondal TK (2015) Influence of drought stress on cellular ultrastructure and antioxidant system in tea cultivars with different drought sensitivities. J Environ Biol 36:875–882

    CAS  PubMed  Google Scholar 

  • Depater S, Pham K, Chua NH, Memelink J, Kijne J (1993) A 22-bp fragment of the pea lectin promoter containing essential TGAClike motifs confers seed-specific gene-expression. Plant Cell 5:877–886

    Article  CAS  Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid-peroxidation. Method Enzymol 186:421–431

    Article  CAS  Google Scholar 

  • 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 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • Gao CY, Li PL, Song AP, Wang HB, Wang YJ, Ren LP, Qi XY, Chen FD, Jiang JF, Chen SM (2015) Isolation and characterization of six AP2/ERF transcription factor genes in Chrysanthemum nankingense. Int J Mol Sci 16:2052–2065

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Guo JK, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang YH, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35:105–118

    Article  CAS  PubMed  Google Scholar 

  • Hobo T, Asada M, Kowyama Y, Hattori T (1999) ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J 19:679–689

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    Article  PubMed  PubMed Central  Google Scholar 

  • Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K (2005) RARTF: database and tools for complete sets of Arabidopsis transcription factors. DNA Res 12:247–256

    Article  CAS  PubMed  Google Scholar 

  • Jaffar MA, Song AP, Faheem M, Chen SM, Jiang JF, Liu C, Fan QQ, Chen FD (2016) Involvement of CmWRKY10 in drought tolerance of Chrysanthemum through the ABA-signaling pathway. Int J Mol Sci 17:693

    Article  PubMed Central  Google Scholar 

  • Jefferson RA (1989) The GUS reporter gene system. Nature 342:837–838

    Article  CAS  PubMed  Google Scholar 

  • Jin C, Huang XS, Li KQ, Yin H, Li LT, Yao ZH, Zhang SL (2016) Overexpression of a bHLH1 transcription factor of Pyrus ussuriensis confers enhanced cold tolerance and increases expression of stress-responsive genes. Front Plant Sci 7:441

    PubMed  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Lei M, Li ZY, Wang JB, Fu YL, Ao MF, Xu L (2016) AfAP2-1, an age-dependent gene of Aechmea fasciata, responds to exogenous ethylene treatment. Int J Mol Sci 17:303

    Article  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li PL, Song AP, Gao CY, Wang LX, Wang YJ, Sun J, Jiang JF, Chen FD, Chen SM (2015) Chrysanthemum WRKY gene CmWRKY17 negatively regulates salt stress tolerance in transgenic chrysanthemum and Arabidopsis plants. Plant Cell Rep 34:1365–1378

    Article  CAS  PubMed  Google Scholar 

  • Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol 3:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu SC, Jin JQ, Ma JQ, Yao MZ, Ma CL, Li CF, Ding ZT, Chen L (2016a) Transcriptomic analysis of tea plant responding to drought stress and recovery. PLoS One 11:e0147306

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu YG, Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674–681

    Article  CAS  PubMed  Google Scholar 

  • Liu ZW, Wu ZJ, Li XH, Huang Y, Li H, Wang YX, Zhuang J (2016b) Identification, classification, and expression profiles of heat shock transcription factors in tea plant (Camellia sinensis) under temperature stress. Gene 576:52–59

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Mukhopadhyay M, Das A, Subba P, Bantawa P, Sarkar B, Ghosh P, Mondal TK (2013) Structural, physiological, and biochemical profiling of tea plantlets under zinc stress. Biol Plantarum 57:474–480

    Article  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    Article  CAS  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P, Hayashizaki Y, Suzuki K, Kojima K, Takahara Y, Yamamoto K, Kikuchi S (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10:239–247

    Article  CAS  PubMed  Google Scholar 

  • Pascual MB, Canovas FM, Avila C (2015) The NAC transcription factor family in maritime pine (Pinus pinaster): molecular regulation of two genes involved in stress responses. BMC Plant Biol 15:254

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in droughtresponsive gene expression. Plant Cell 18:1292–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan DP, Huang JG, Yang YT, Guo YH, Wu CA, Yang GD, Gao Z, Zheng CC (2007) Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytol 176:70–81

    Article  CAS  PubMed  Google Scholar 

  • Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  PubMed  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456

    Article  CAS  PubMed  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/ helix-loop-helix transcription factor family. Plant Cell 15:1749–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verdaguer B, de Kochko A, Fux CI, Beachy RN, Fauquet C (1998) Functional organization of the cassava vein mosaic virus (CsVMV) promoter. Plant Mol Biol 37:1055–1067

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Wang YC, Cao HL, Hao XY, Zeng JM, Yang YJ, Wang XC (2016a) Transcriptome analysis of an anthracnose-resistant tea plant cultivar reveals genes associated with resistance to Colletotrichum camelliae. PLoS One 11:e0148535

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang QY, Guan YC, Wu YR, Chen HL, Chen F, Chu CC (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602

    Article  CAS  PubMed  Google Scholar 

  • Wang WD, Wang YH, Du YL, Zhao Z, Zhu XJ, Jiang X, Shu ZF, Yin Y, Li XH (2014) Overexpression of Camellia sinensis H1 histone gene confers abiotic stress tolerance in transgenic tobacco. Plant Cell Rep 33:1829–1841

    Article  CAS  PubMed  Google Scholar 

  • Wang WD, Xin HH, Wang ML, Ma QP, Wang L, Kaleri NA, Wang YH, Li XH (2016b) Transcriptomic analysis reveals the molecular mechanisms of drought-stress-induced decreases in Camellia sinensis leaf quality. Front Plant Sci 7:385

    PubMed  PubMed Central  Google Scholar 

  • Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ, Jin JQ, Li X, Yang YJ (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics 14:415

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang XM, Dong J, Liu Y, Gao HW (2010) A novel dehydrationresponsive element-binding protein from Caragana korshinskii is involved in the response to multiple abiotic stresses and enhances stress tolerance in transgenic tobacco. Plant Mol Biol Rep 28:664–675

    Article  Google Scholar 

  • Wang YN, Tang L, Hou Y, Wang P, Yang H, Wei CL (2016c) Differential transcriptome analysis of leaves of tea plant (Camellia sinensis) provides comprehensive insights into the defense responses to Ectropis oblique attack using RNA-Seq. Functional & Integrative Genomics 16:383–398

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wu CY, Suzuki A, Washida H, Takaiwa F (1998) The GCN4 motif in a rice glutelin gene is essential for endosperm-specific gene expression and is activated by Opaque-2 in transgenic rice plants. Plant J 14:673–683

    Article  CAS  PubMed  Google Scholar 

  • Wu ZJ, Li XH, Liu ZW, Li H, Wang YX, Zhuang J (2015) Transcriptomebased discovery of AP2/ERF transcription factors related to temperature stress in tea plant (Camellia sinensis). Functional & Integrative Genomics 15:741–752

    Article  CAS  Google Scholar 

  • Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABAindependent pathways. Planta 233:219–229

    Article  CAS  PubMed  Google Scholar 

  • Zhang LR, Xing D (2008) Methyl jasmonate induces production of reactive oxygen species and alterations in mitochondrial dynamics that precede photosynthetic dysfunction and subsequent cell death. Plant Cell Physiol 49:1092–1111

    Article  CAS  PubMed  Google Scholar 

  • Zhang XR, Henriques R, Lin SS, Niu QW, Chua NH (2006) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat Protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhao T, Liang D, Wang P, Liu JY, Ma FW (2012a) Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Mol Genet Genomics 287:423–436

    Article  CAS  PubMed  Google Scholar 

  • Zhao XJ, Lei HJ, Zhao K, Yuan HZ, Li TH (2012b) Isolation and characterization of a dehydration responsive element binding factor MsDREBA5 in Malus sieversii Roem. Sci Hortic 142:212–220

    Article  CAS  Google Scholar 

  • Zhou W, Jia CG, Wu X, Hu RX, Yu G, Zhang XH, Liu JL, Pan HY (2016) ZmDBF3, a novel transcription factor from Maize (Zea mays L.), is involved in multiple abiotic stress tolerance Plant Mol Biol Rep 34:353–364

    Article  CAS  Google Scholar 

  • Zhuang J, Cai B, Peng RH, Zhu B, Jin XF, Xue Y, Gao F, Fu XY, Tian YS, Zhao W, Qiao YS, Zhang Z, Xiong AS, Yao QH (2008) Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Biophys Res Commun 371:468–474

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xinghui Li.

Electronic supplementary material

12374_2016_547_MOESM1_ESM.docx

Overexpression of a Camellia sinensis DREB transcription factor gene (CsDREB) increases salt and drought tolerance in transgenic Arabidopsis thaliana

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, M., Zhuang, J., Zou, Z. et al. Overexpression of a Camellia sinensis DREB transcription factor gene (CsDREB) increases salt and drought tolerance in transgenic Arabidopsis thaliana . J. Plant Biol. 60, 452–461 (2017). https://doi.org/10.1007/s12374-016-0547-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0547-9

Keywords

Navigation