Skip to main content
SpringerLink
Log in

Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Ethylene responsive factors (ERFs) are important in regulating plant pathogen resistance, abiotic stress tolerance and plant development. Recent studies have greatly enlarged the ERF protein family and revealed more important roles of ERFs in plants. Here, we report our finding of a tomato ERF protein TSRF1, which is transcriptionally up-regulated by ethylene, salicylic acid, or Ralstonia solanacearum strain BJ1057 infection. Biochemical analysis indicates that TSRF1 specifically interacts in vitro with the GCC box, an element present in the promoters of many pathogenesis-related (PR) genes. Further investigation evidences that TSRF1 activates in vivothe expression of reporter β-glucuronidase gene controlled by GCC box. More importantly, overexpressing TSRF1 in tobacco and tomato constitutively activates the expression of PR genes, and subsequently enhancing transgenic plant resistance to the bacterial wilt caused by Ralstonia solanacearum strain BJ1057. Therefore our investigation not only extends the functions of ERF proteins in plant resistance to R. solanacearum, but also provides further clues to understanding the mechanism of host regulatory proteins in response to the infection of pathogens.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

    Google Scholar 

  • Buttner, M. and Singh, K.B. 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.

    Google Scholar 

  • Chakravarthy, S., Tuori, R.P., D'Ascenzo, M.D., Fobert, P.R., Despres, C. and Martin, G.B. 2003. The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 15: 3033–3050.

    Google Scholar 

  • Danhash, N., Wagemakers, C.A.M., van Kan, J.A.L. and de Wit, P.J.G.M. 1993. Molecular characterization of four chitinase cDNAs obtained from Cladosporium fulvum-infected tomato. Plant Mol. Biol. 22: 1017–1029.

    Google Scholar 

  • Deslandes, L., Olivier, J., Peeters, N., Feng, D.X., Khounlotham, M., Boucher, C., Somssich, I., Genin, S. and Marco, Y. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. USA 100: 8024–8029.

    Google Scholar 

  • Deslandes, L., Olivier, J., Theulieres, F., Hirsch, J., Feng, D.X., Bittner-Eddy, P., Beynon, J. and Marco, Y. 2002. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. USA 99: 2404–2409.

    Google Scholar 

  • Dong, X. 1998. SA, JA, ethylene and disease resistance in plants. Curr. Opin. Plant Biol. 1: 316–323.

    Google Scholar 

  • Eyal, Y., Meller, Y., Lev-Yadum, S. and Fluhr, R. 1993. A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J. 4: 225–234.

    Google Scholar 

  • Eyal, Y., Sagee, O. and Fluhr, R. 1992. Dark-induced accumulation of a basic pathogenesis-related (PR-1) transcript and a light requirement for its induction by ethylene. Plant Mol. Biol. 19: 589–599.

    Google Scholar 

  • Fujimoto, S.Y., Ohta, M., Usui, A., Shinshi, H. and Ohme-Takagi, M. 2000. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors ofGCCbox-mediated gene expression. Plant Cell 12: 393–404.

    Google Scholar 

  • Fukuda, Y., Ohme, M. and Shinshi, H. 1991. Gene structure and expression of a tobacco endochitinase gene in suspension-cultured tobacco cells. Plant Mol. Biol. 16: 1–10.

    Google Scholar 

  • Gu, Y.-Q., Wildermuth, M.C., Chakravarthy, S., Loh, Y.T., Yang, C., He, X., Han, Y. and Martin, G.B. 2002. Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 14: 817–831.

    Google Scholar 

  • Gu, Y.-Q., Yang, C., Thara, V.K., Zhou, J. and Martin, G.B. 2000. Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 12: 771–785.

    Google Scholar 

  • Guo, H. and Ecker, J.R. 2004. The ethylene signaling pathway: new insights. Curr. Opin. Plant Biol. 7: 40–49.

    Google Scholar 

  • Gutterson, N. and Reuber, T.L. 2004. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr. Opin. Plant Biol. 7: 465–471.

    Google Scholar 

  • He, L.Y., Sequeira, L. and Kelman, A. 1983. Characteristics of strains of Pseudomonas solanacearum from China. Plant Dis. 12: 1357–1361.

    Google Scholar 

  • He, P., Warren, R.F., Zhao, T., Shan, L., Zhu, L., Tang, X. and Zhou, J.M. 2001. Overexpression of Pti5 in tomato potentiates pathogen-induced defense gene expression and enhances disease resistance to Pseudomonas syringae pv tomato. Mol. Plant Microbe. Interact. 14: 1453–1457.

    Google Scholar 

  • Hoekema, A., Hirsch, P., Hooykaas, P.J.J. and Schilperoort, R. 1983. A binary plant vector strategy based on separation of virand T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303: 179–180.

    Google Scholar 

  • Hua, J. and Meyerowitz, E.M. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94: 261–271.

    Google Scholar 

  • Jia, Y. and Martin, G.B. 1999. Rapid transcript accumulation of pathogenesis-related genes during an incompatible interaction in bacterial speck disease-resistant tomato plants. Plant Mol. Biol. 40: 455–465.

    Google Scholar 

  • Kieber, J.J., Rothenberg, M., Roman, G., Feldmann, K.A. and Ecker, J.R. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72: 427–441.

    Google Scholar 

  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and 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-temperatureresponsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391–1406.

    Google Scholar 

  • Lorenzo, O., Piqueras, R., Sanchez-Serrano, J.J. and Solano, R. 2003. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165–178.

    Google Scholar 

  • Martin, G.B., Brommonschenkel, S., Chunwongse, J., Frary, A., Ganal, M.W., Spivey, R., Wu, T., Earle, E.D. and Tanksley, S.D. 1993. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262: 1432–1436.

    Google Scholar 

  • Menke, F.L., Champion, A., Kijne, J.W. and Memelink, J. 1999. A novel jasmonate-and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate-and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J. 18: 4455–4463.

    Google Scholar 

  • Niu, X., Helentjaris, T. and Bate, N.J. 2002. Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14: 2565–2575.

    Google Scholar 

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

    Google Scholar 

  • Ohta, M., Ohme-Takagi, M. and Shinshi, H. 2000. Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J. 22: 29–38.

    Google Scholar 

  • Park, J.M., Park, C.J., Lee, S.B., Ham, B.K., Shin, R. and Paek, K.H. 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.

    Google Scholar 

  • Pastuglia, M., Roby, D., Dumas, C. and Cock, J.M. 1997. Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9: 49–60.

    Google Scholar 

  • Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J.C., Cattolico, L., Chandler, M., Choisne, N., Claudel-Renard, C., Cunnac, S., Demange, N., Gaspin, C., Lavie, M., Moisan, A., Robert, C., Saurin, W., Schiex, T., Siguier, P., Thebault, P., Whalen, M., Wincker, P., Levy, M., Weissenbach, J. and Boucher, C.A. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 414: 497–502.

    Google Scholar 

  • Sessa, G., Meller, Y. and 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.

    Google Scholar 

  • Shinshi, H., Usami, S. and Ohme-Takagi, M. 1995. Identification of an ethylene-responsive region in the promoter of a tobacco class I chitinase gene. Plant Mol. Biol. 27: 923–932.

    Google Scholar 

  • Solano, R., Stepanova, A., Chao, Q. and Ecker, J.R. 1998. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12: 3703–3714.

    Google Scholar 

  • Sperisen, C., Ryals, J. and Meins, F. 1991. Comparison of cloned genes provides evidence for intergenomic exchange of DNA in the evolution of a tobacco glucan endo-1, 3-betaglucosidase gene family. Proc. Natl. Acad. Sci. U.S.A. 88: 1820–1824.

    Google Scholar 

  • Stockinger, E.J., Gilmour, A.J. and Thomashow, M.F. 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.

    Google Scholar 

  • Thilmony, R.L., Chen, Z., Bressan, R.A. and Martin, G.B. 1995. Expression of the tomato Pto gene in tobacco enhances resistance to Pseudomonas syringae pv tabaci expressing avrPto. Plant Cell 7: 1529–1536.

    Google Scholar 

  • Tournier, B., Sanchez-Ballesta, M.T., Jones, B., Pesquet, E., Regad, F., Latche, A., Pech, J.C. and 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.

    Google Scholar 

  • van der Fits, L. and Memelink, J. 2000. ORCA3, a jasmonateresponsive transcriptional regulator of plant primary and secondary metabolism. Science 289: 295–297.

    Google Scholar 

  • van der Fits, L. and Memelink, J. 2001. The jasmonateinducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonateresponsive promoter element. Plant J. 25: 43–53.

    Google Scholar 

  • van Kan, J.A., Cozijnsen, T., Danhash, N. and de Wit, P.J. 1995. Induction of tomato stress protein mRNAs by ethephon, 2,6-dichloroisonicotinic acid and salicylate. Plant Mol. Biol. 27: 1205–1213.

    Google Scholar 

  • van Kan, J.A., Joosten, M.H., Wagemakers, C.A., van den Berg-Velthuis, G.C. and de Wit, P.J. 1992. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum. Plant Mol. Biol. 20: 513–527.

    Google Scholar 

  • Wang, H., Huang, Z., Chen, Q., Zhang, Z., Zhang, H., Wu, Y., Huang, D. and Huang, R. 2004. Ectopic overexpression of tomato JERF3 in tobacco activates downstream gene expression and enhances salt tolerance. Plant Mol. Biol. (in press)

  • Wang, K.L., Li, H. and Ecker, J.R. 2002. Ethylene biosynthesis and signaling networks. Plant Cell 14 (Suppl): S131–S151.

    Google Scholar 

  • Xiong, L. and Zhu, J.K. 2003. Regulation of abscisic acid biosynthesis. Plant Physiol. 133: 29–36.

    Google Scholar 

  • Zhou, J., Tang, X. and Martin, G.B. 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.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The National Plant Gene Research Center (Beijing), Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Hongbo Zhang, Zejun Huang, Dafang Huang & Rongfeng Huang

  2. National Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, 100094, China

    Hongbo Zhang, Jia Chen & Xue-Chen Wang

  3. Biotechnology Research Center, Shanghai Academy of Agricultural Sciences, Shanghai, 201106, China

    Dabing Zhang & Yuhong Yang

Authors
  1. Hongbo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dabing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jia Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yuhong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zejun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dafang Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xue-Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rongfeng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, H., Zhang, D., Chen, J. et al. Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum . Plant Mol Biol 55, 825–834 (2004). https://doi.org/10.1007/s11103-004-2140-8

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-2140-8

Search

Navigation