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Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance

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Abstract

ERF transcription factors play important roles in regulating gene expression under abiotic and biotic stresses. The first member of the ERF gene family in wheat (Triticum aestivum L.) was isolated by screening a drought-induced cDNA library and designated as T. aestivum ethylene-responsive factor 1 (TaERF1), which encoded a putative protein of 355 amino acids with a conserved DNA-binding domain and a conserved N-terminal motif (MCGGAIL). The TaERF1 gene was located on chromosome 7A. Protein interaction assays indicated that TaERF1, with a putative phosphorylation site (TPDITS) in the C-terminal region, was a potential phosphorylation substrate for TaMAPK1 protein kinase. Deletion of the N-terminal motif enhanced the interaction of TaERF1 with TaMAPK1. The predicted TaERF1 protein contained three putative nuclear localization signals (NLSs), and three NLSs modulated synergistically the activity of subcellular localization. As a trans-acting factor, TaERF1 was capable of binding to the GCC-box and CRT/DRE elements in vitro, and of trans-activating reporter gene expression in tobacco (Nicotiana tabacum L.) leaves. Transcription of the TaERF1 gene was induced not only by drought, salinity and low-temperature stresses and exogenous ABA, ethylene and salicylic acid, but also by infection with Blumeria graminis f. sp. tritici. Furthermore, overexpression of TaERF1 activated stress-related genes, including PR and COR/RD genes, under normal growth conditions, and improved pathogen and abiotic stress tolerance in transgenic plants. These results suggested that the TaERF1 gene encodes a GCC-box and CRT/DRE element binding factor that might be involved in multiple stress signal transduction pathways.

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Abbreviations

ABA:

abscisic acid

COR/RD :

cold-regulated/responsive to dehydration

CRT/DRE:

C-repeat/dehydration-responsive element

DREB:

CRT/DRE binding protein

EMSA:

electrophoretic mobility shift assays

ERF:

ethylene-responsive factor

MAPK:

mitogen-activated protein kinase

NLS:

nuclear localization signal

PR:

pathogenesis-related

SA:

salicylic acid

References

  • Abeles FB, Morgan PW, Saltveit Jr ME (1992) Ethylene in Plant Biology, 2nd edn. Academic Press, New York

    Google Scholar 

  • Agrawal GK, Agrawal SK, Shibato J, Iwahashi H, Rakwal R (2003) Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys Res Commun 300:775–783

    Article  PubMed  CAS  Google Scholar 

  • Aono M, Kubo A, Saji H, Tanaka K, Kondo N (1993) Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with high chloroplastic glutathione reductase activity. Plant Cell Physiol 34:129–136

    CAS  Google Scholar 

  • Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32

    Article  PubMed  CAS  Google Scholar 

  • Broekaert WF, Delaure SL, De Bolle MF, Cammue BP (2006) The role of ethylene in host-pathogen interactions. Annu Rev Phytopathol 44:393–416

    Article  PubMed  CAS  Google Scholar 

  • Buttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci USA 94:5961–5966

    Article  PubMed  CAS  Google Scholar 

  • Cao YF, Song FM, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163:1167–1178

    Article  PubMed  CAS  Google Scholar 

  • Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972

    Article  PubMed  CAS  Google Scholar 

  • Fischer U, Droge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Interact 17:1162–1171

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box mediated gene expression. Plant Cell 12:393–404

    Article  PubMed  CAS  Google Scholar 

  • Gu YQ, Wildermuth MC, Chakravarthy S, Loh YT, Yang C, He X, Han Y, Martin GB (2002) Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14:817–831

    Article  PubMed  CAS  Google Scholar 

  • Gu YQ, Yang C, Thara VK, Zhou J, Martin GB (2000) Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12:771–785

    Article  PubMed  CAS  Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49

    Article  PubMed  CAS  Google Scholar 

  • Ham BK, Park JM, Lee SB, Kim MJ, Lee IJ, Kim KJ, Kwon CS, Paek KH (2006) Tobacco Tsip1, a DnaJ-type Zn finger protein, is recruited to and potentiates Tsi1-mediated transcriptional activation. Plant Cell 18:2005–2020

    Article  PubMed  CAS  Google Scholar 

  • Hossain KG, Kalavacharla V, Lazo GR, Hegstad J, Wentz MJ, Kianian PM, Simons K, Gehlhar S, Rust JL, Syamala RR, Obeori K, Bhamidimarri S, Karunadharma P, Chao S, Anderson OD, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Akhunov ED, Dvorak J, Miftahudin RK, Gustafson JP, Radhawa HS, Dilbirligi M, Gill KS, Peng JH, Lapitan NL, Greene RA, Bermudez-Kandianis CE, Sorrells ME, Feril O, Pathan MS, Nguyen HT, Gonzalez-Hernandez JL, Conley EJ, Anderson JA, Choi DW, Fenton D, Close TJ, McGuire PE, Qualset CO, Kianian SF (2004) A chromosome bin map of 2148 expressed sequence tag loci of wheat homoeologous group 7. Genetics 168:687–699

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573:110–116

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y, Hwang I, Kim M (2007) The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 225:575–588

    Article  PubMed  CAS  Google Scholar 

  • Koyama T, Okada T, Kitajima S, Ohme-Takagi M, Shinshi H, Sato F (2003) Isolation of tobacco ubiquitin-conjugating enzyme cDNA in a yeast two-hybrid system with tobacco ERF3 as bait and its characterization of specific interaction. J Exp Bot 54:1175–1181

    Article  PubMed  CAS  Google Scholar 

  • Lee JH, Hong JP, Oh SK, Lee S, Choi D, Kim WT (2004) The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant Mol Biol 55:61–81

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Ogawa T, Pan L, Kawai-Yamada M, Yu LH, Yamamura S, Koyama T, Kitajima S, Ohme-Takagi M, Sato F, Uchimiya H (2005) Functional analysis of Arabidopsis ethylene-responsive element binding protein conferring resistance to Bax and abiotic stress-induced plant cell death. Plant Physiol 138:1436–1445

    Article  PubMed  CAS  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  PubMed  CAS  Google Scholar 

  • Onate-Sanchez L, Singh KB (2002) Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection. Plant Physiol 128:1313–1322

    Article  PubMed  CAS  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    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 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Habor: Cold Spring Harbor Laboratory Press

  • Schoenbeck MA, Samac DA, Fedorova M, Gregerson RG, Gantt JS, Vance CP (1999) The alfalfa (Medicago sativa) TDY1 gene encodes a mitogen-activated protein kinase homolog. Mol Plant Microbe Interact 12:882–893

    Article  PubMed  CAS  Google Scholar 

  • Sessa G, Meller Y, Fluhr R (1995) A GCC element and a G-box motif participate in ethylene-induced expression of the PRB-1b gene. Plant Mol Biol 28:145–153

    Article  PubMed  CAS  Google Scholar 

  • Shin R, Park JM, An JM, Paek KH (2002) Ectopic expression of Tsi1 in transgenic hot pepper plants enhances host resistance to viral, bacterial, and oomycete pathogens. Mol Plant Microbe Interact 15:983–989

    Article  PubMed  CAS  Google Scholar 

  • Song CP, Galbraith DW (2006) AtSAP18, an orthologue of human SAP18, is involved in the regulation of salt stress and mediates transcriptional repression in Arabidopsis. Plant Mol Biol 60:241–257

    Article  PubMed  CAS  Google Scholar 

  • Song CP, Agarwal M, Ohta M, Guo Y, Halfter U, Wang P, Zhu JK (2005) Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17:2384–2396

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    Article  PubMed  CAS  Google Scholar 

  • Tang M, Sun J, Liu Y, Chen F, Shen S (2007) Isolation and functional characterization of the JcERF gene, a putative AP2/EREBP domain-containing transcription factor, in the woody oil plant Jatropha curcas. Plant Mol Biol 63:419–428

    Article  PubMed  CAS  Google Scholar 

  • Thilmony RL, Chen Z, Bressan RA, Martin GB (1995) Expression of the tomato Pto gene in tobacco enhances resistance to Pseudomonas syringae pv tabaci expressing avrPto. Plant Cell 7:1529–1536

    Article  PubMed  CAS  Google Scholar 

  • Tournier B, Sanchez-Ballesta MT, Jones B, Pesquet E, Regad F, Latche A, Pech JC, Bouzayen M (2003) New members of the tomato ERF family show specific expression pattern and diverse DNA-binding capacity to the GCC box element. FEBS Lett 550:149–154

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell (Suppl) 14:165–183

    Google Scholar 

  • Yang YN, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58:585–596

    Article  PubMed  CAS  Google Scholar 

  • Yap YK, Kodama Y, Waller F, Chung KM, Ueda H, Nakamura K, Oldsen M, Yoda H, Yamaguchi Y, Sano H (2005) Activation of a novel transcription factor through phosphorylation by WIPK, a wound-induced mitogen-activated protein kinase in tobacco plants. Plant Physiol 139:127–137

    Article  PubMed  CAS  Google Scholar 

  • Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, Choi D (2004) The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol 136:2862–2874

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Huang Z, Xie B, Chen Q, Tian X, Zhang X, Zhang H, Lu X, Huang D, Huang R (2004) The ethylene-, jasmonate-, abscisic acid- and NaCl-responsive tomato transcription factor JERF1 modulates expression of GCC box-containing genes and salt tolerance in tobacco. Planta 220:262–270

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Tang X, Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16:3207–3218

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the National “863” High-tech Project (2006AA10Z1E9 and 2007AA10Z130), National Special Project for Transgenic Plants and Industry (JY03-A-18-01) and National Natural Science Foundation of China (30700504). We are grateful to Dr. Han F.P. (Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Canada) for providing the nullisomic-tetrasomics of T. aestivum L. cv. Chinese Spring, Dr. Wang D.W. (Institute of Genetics, Chinese Academy of Sciences, China) for providing the hGFP vector, Dr Chen F. (Institute of Development, Chinese Academy of Sciences, China) for constructing the wheat cDNA library, and Dr McIntosh R.A. (Plant Breeding Institute, University of Sydney, Australia) for critically reading the manuscript.

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Authors and Affiliations

  1. National Key Facility of Crop Gene Resources and Genetic Improvement (NFCRI), Key Laboratory of Crop Genetics and Breeding, Ministry of Agriculture, Institute of Crop Science, Chinese Academy of Agriculture Sciences (CAAS), Beijing, 100081, P.R. China

    Zhao-Shi Xu, Lan-Qin Xia, Ming Chen, Rui-Yue Zhang, Lian-Cheng Li, Yun-Xiang Zhao, Yan Lu, Zhi-Yong Ni, Li Liu, Zhi-Gang Qiu & You-Zhi Ma

  2. Institute of Natural Resources and Regional Planning, Chinese Academy of Agriculture Sciences (CAAS), Beijing, 100081, P.R. China

    Xian-Guo Cheng

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  1. Zhao-Shi Xu
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  2. Lan-Qin Xia
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  3. Ming Chen
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Correspondence to You-Zhi Ma.

Additional information

The nucleotide sequences reported in this paper have been submitted to the GenBank database under accession numbers AY781352 (TaERF1) and AY881102 (TaMAPK1).

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Xu, ZS., Xia, LQ., Chen, M. et al. Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65, 719–732 (2007). https://doi.org/10.1007/s11103-007-9237-9

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