Plant Molecular Biology

, Volume 51, Issue 1, pp 21–37 | Cite as

Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response

Article

Abstract

WRKY proteins are a recently identified class of DNA-binding proteins that recognize the TTGAC(C/T) W-box elements found in the promoters of a large number of plant defense-related genes. With oligo molecules containing the W-box sequences as probes, we detected a number of WRKY DNA-binding activities in Arabidopsis that were induced by salicylic acid (SA). Search of the Arabidopsis genome identifies 72 genes encoding proteins characteristic of WRKY DNA-binding transcription factors that can be divided into three groups based on the number and structures of their WRKY zinc-finger motifs. Northern blotting analysis revealed that 49 of the 72 AtWRKY genes were differentially regulated in the plants infected by an avirulent strain of the bacterial pathogen Pseudomonas syringae or treated by SA. These pathogen- and/or SA-regulated WRKY genes can be further categorized into groups based on their expression patterns in both wild-type plants and mutants defective in defense signaling pathways. Inspection of the 5′ sequences upstream of the predicated translation start sites revealed a substantial enrichment of W boxes in the promoters of pathogen- and/or SA-regulated Arabidopsis WRKY genes. These results suggest that defense-regulated expression of WRKY genes involves extensive transcriptional activation and repression by its own members of the transcription factor superfamily.

Arabidopsis plant defense responses W boxes WRKY proteins 

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References

  1. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815.Google Scholar
  2. Bechtold, N. and Pelletier, G. 1998. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Meth. Mol. Biol. 82: 259–266.Google Scholar
  3. Bent, A.F., Kunkel, B.N., Dahlbeck, D., Brown, K.L., Schmidt, R., Giraudat, J., Leung, J. and Staskawicz, B.J. 1994. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860.Google Scholar
  4. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S. and Dong, X. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63.Google Scholar
  5. Chen, C. and Chen, Z. 2000. Isolation and characterization of two pathogen-and salicylic acid-induced genes encoding WRKY DNA-binding proteins from tobacco. Plant Mol. Biol. 42: 387–396.Google Scholar
  6. Delaney, T.P.U.S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E. and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247–1250.Google Scholar
  7. Dellagi, A., Helibronn, J., Avrova, A.O., Montesano, M., Palva, E.T., Stewart, H.E., Toth, I.K., Cooke, D.E., Lyon, G.D. and Birch, P.R. 2000. A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with class I endochitinase expression. Mol. Plant-Microbe Interact. 13: 1092–1101.Google Scholar
  8. de Pater, S., Greco, V., Pham, K., Memelink, J. and Kijne, J. 1996. Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucl. Acids Res. 24: 4624–4631.Google Scholar
  9. Du, L. and Chen, Z. 2000. Identification of genes encoding novel receptor-like protein kinases as possible target genes of pathogen-induced WRKY DNA-binding proteins. Plant J. 24: 837–848.Google Scholar
  10. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863–14838.Google Scholar
  11. Eulgem, T., Rushton, P.J., Schmelzer, E., Hahlbrock, K. and Somssich, I.E. 1999. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J. 18: 4689–4899.Google Scholar
  12. Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5: 199–206.Google Scholar
  13. Gaffney, T.F.L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H. and Ryals, J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756.Google Scholar
  14. Green, P.J., Kay, S.A. and Chua, N.H. 1987. Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcS-3A gene. EMBO J. 6: 2543–2549.Google Scholar
  15. Hara, K., Yagi, M., Kusano, T. and Sano, H. 2000. Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol. Gen. Genet. 263: 30–37.Google Scholar
  16. Ishiguro, S. and Nakamura, K. 1994. Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and ?-amylase from sweet potato. Mol. Gen. Genet. 244: 563–571.Google Scholar
  17. Khorasanizadeh, S. and Rastinejad, F. 2001. Nuclear-receptor interactions on DNA-response elements. Trends Biochem. Sci. 26: 384–390.Google Scholar
  18. Kim, C.Y., Lee, S.H., Park, H.C., Bae, C.G., Cheong, Y.H., Choi, Y.J., Han, C., Lee, S.Y., Lim, C.O. and Cho, M.J. 2000. Identification of rice blast fungal elicitor-responsive genes by differential display analysis. Mol. Plant-Microbe Interact. 13: 470–474.Google Scholar
  19. Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Bevan, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J. and Weisshaar, B. 1998. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16: 263–276.Google Scholar
  20. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K.A., Dangl, J.L. and Dietrich, R.A. 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet. 26: 403–410.Google Scholar
  21. Page, R.D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357–358.Google Scholar
  22. Rastinejad, F. 2001. Retinoid X receptor and its partners in the nuclear receptor family. Curr. Opin. Struct. Biol. 11: 33–38.Google Scholar
  23. Rushton, P.J. and Somssich, I.E. 1998. Transcriptional control of plant genes responsive to pathogens. Curr. Opin. Plant Biol. 1: 311–315.Google Scholar
  24. Rushton, P.J., Macdonald, H., Huttly, A.K., Lazarus, C.M. and Hooley, R. 1995. Members of a new family of DNA-binding proteins bind to a conserved cis element in the promoters of ?-Amy2 genes. Plant Mol. Biol. 29: 691–702.Google Scholar
  25. Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K. and Somssich, I.E. 1996. Interaction of elicitor-induced DNAbinding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15: 5690–5700.Google Scholar
  26. Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.Google Scholar
  27. Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.Google Scholar
  28. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. 1997. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25: 4876–4882.Google Scholar
  29. Wang, Z., Yang, P., Fan, B. and Chen, Z. 1998. An oligo selection procedure for identification of sequence-specific DNA-binding activities associated with the plant defence response. Plant J. 16: 515–522.Google Scholar
  30. Yang, P., Wang, Z., Fan, B., Chen, C. and Chen, Z. 1999. A pathogen-and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J. 18: 141–149.Google Scholar
  31. Yang, Y., Shah, J. and Klessig, D.F. 1997. Signal perception and transduction in plant defense responses. Genes Dev. 11: 1621–1639.Google Scholar
  32. Yu, D., Liu, Y., Fan, B., Klessig, D. and Chen, Z. 1997. Is the high basal levels of salicylic acid important for disease resistance in potato? Plant Physiol. 115: 343–349.Google Scholar
  33. Yu, L., Chen, C. and Chen, Z. 2001. Evidence for an important role of theWRKY DNA-binding proteins in the regulation of the NPR1 gene expression. Plant Cell 13: 1527–1539.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Biotechnology InstituteZhejiang University, HangzhouZhejiangChina
  2. 2.Department of Microbiology, Molecular Biology and BiochemistryUniversity of IdahoMoscow

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