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SIVB 2003 Congress Symposium Proceeding: Plant-Targets of Pathogenic Effectors Can Transduce Both Virulence and Resistance Signals

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Summary

Pathogens of plants produce effector proteins necessary for successful parasitism. The effectors enhance pathogen virulence by manipulating signaling in the plant. Plants produce resistance (R) proteins that mediate recognition of specific effectors and respond by initiating plant defenses. In many cases, R-proteins perceive effectors indirectly; virulence signaling initiated by the effector is shunted, via the R-protein, into a resistance response. Therefore, by understanding how effectors manipulate virulence targets we will concurrently gain insight into how this signaling elicits R-protein-mediated defense responses.

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References

  • Axtell, M. J.; Chisholm, S. T.; Dahlbeck, D.; Staskawicz, B. J. Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol. Microbiol. 49:1537–1546; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Axtell, M. J.; Staskawicz, B. J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Bent, A. F.; Kunkel, B. N.; Dahlbeck, D.; Brown, K. L.; Schmidt, R.; Giraudat, J.; Leung, J.; Staskawicz, B. J. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856–1860; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Bisgrove, S. R.; Simonich, M. T.; Smith, N. M.; Sattler, N. M.; Innes, R. W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927–933; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Boyes, D. C.; Nam, J.; Dangl, J. L. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl Acad. Sci. USA 95:15849–15854; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Chen, Z.; Kloek, A. P.; Boch, J.; Katagiri, F.; Kunkel, B. N. The Pseudomonas syringae avrRpt2 gene product promotes pathogenicity from inside the plant cell. Mol. Plant-Microbe Interact. 13:1312–1321; 2000.

    PubMed  CAS  Google Scholar 

  • Collmer, A.; Lindeberg, M.; Petnicki-Ocwieja, T.; Schnieder, D. J.; Alfano, J. R. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462–469; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Dangl, J. L.; Jones, J. D. G. Plant pathogens and integrated defence responses to infection. Nature 411:826–833; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Dixon, M. S.; Golstein, C.; Thomas, C. M.; van Der Biezen, E. A.; Jones, J. D. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. Proc. Natl Acad. Sci. USA 97:8807–8814; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Ellis, J.; Dodds, P.; Pryor, T. Structure, function, and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3:278–284; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Gálan, J. E.; Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322–1328; 1999.

    Article  PubMed  Google Scholar 

  • Grant, M. R.; Godiard, L.; Straube, E.; Ashfield, T.; Lewald, J.; Sattler, A.; Innes, R. W.; Dangl, J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843–846; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Guttman, D. S.; Greenberg, J. T. Functional analysis of the Type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant Pathol. 14:145–155; 2001.

    CAS  Google Scholar 

  • Hammond-Kosack, K. E.; Parker, J. E. Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14:177–193; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Holt, B. F., 3rd; Mackey, D.; Dangl, J. L. Recognition of pathogens by plants. Curr. Biol. 10:R5–7; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Janeway, C. A., Jr.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20:197–216; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Jia, Y.; McAdams, S. A.; Bryan, G. T.; Hershey, H. P.; Valent, B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19:4004–4014; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y. J.; Lin, N.-C.; Martin, G. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–596; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Kruger, J.; Thomas, C. M.; Golstein, C.; Dixon, M. S.; Smoker, M.; Tang, S.; Mulder, L.; Jones, J. D. G. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296:744–747; 2002.

    Article  PubMed  Google Scholar 

  • Langford, A. N. Autogenous necrosis in tomatoes immune from Cladosporium fulvum Cooke. Can. J. Res. 26:35–64; 1948.

    Google Scholar 

  • Mackey, D.; Belkhadir, Y.; Alonso, J. M.; Ecker, J. R.; Dangl, J. L. Arabidopsis RIN4 is a target of the Type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Mackey, D.; Holt III, B. F.; Wiig, A.; Dangl, J. L. RIN4 interacts with Pseudomonas syringae Type III effector molecules and is required for RPM1-mediated disease resistance in Arabidopsis. Cell 108:743–754; 2002.

    Article  PubMed  CAS  Google Scholar 

  • McDowell, J. M.; Woffenden, B. J. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21:178–183; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Nimchuk, Z.; Marois, E.; Kjemtrup, S.; Leister, R. T.; Katagiri, F.; Dangl, J. L. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several Type III effector proteins from Pseudomonas syringae. Cell 101:353–363; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Nimchuk, Z.; Rohmer, L.; Chang, J. H.; Dangl, J. L. Knowing the dancer from the dance: R gene products and their interactions with other proteins from host and pathogen. Curr. Opin. Plant Biol. 4:288–294; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Nurnberger, T.; Brunner, F. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5:318–324; 2002.

    Article  PubMed  Google Scholar 

  • Osman, H.; Vauthrin, S.; Mikes, V.; Milat, M. L.; Panahieres, F.; Marais, A.; Brunie, S.; Maume, B.; Ponchet, M.; Blein, J. P. Mediation of elicitin activity on tobacco is assumed by elicitin-sterol complexes. Mol. Biol. Cell 12:2825–2834; 2001.

    PubMed  CAS  Google Scholar 

  • Reuber, T. L.; Ausubel, F. M. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPM1 disease resistance genes. Plant Cell 8:241–249; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Ritter, C.; Dangl, J. L. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. Plant—Microbe Interact. 8:444–453; 1995.

    PubMed  CAS  Google Scholar 

  • Ritter, C.; Dangl, J. L. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8:251–257; 1996.

    Article  PubMed  CAS  Google Scholar 

  • Rohmer, L.; Kjemtrup, S.; Marchesini, P.; Dangl, J. L. Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Mol. Microbiol. 47:1545–1562; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Shao, F.; Golstein, C.; Ade, J.; Stoutemyer, M.; Dixon, J. E.; Innes, R. W. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233; 2003.

    Article  PubMed  CAS  Google Scholar 

  • Shao, F.; Merritt, P. M.; Bao, Z.; Innes, R. W.; Dixon, J. E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575–588; 2002.

    Article  PubMed  CAS  Google Scholar 

  • The Arabidopsis Genome Initiative. Analysis of the genome of the flowering plant Arabidopsis thaliana. Nature 408:796–815; 2000.

    Article  Google Scholar 

  • Thomma, B. P. H. J.; Penninckx, I. A. M. A.; Cammue, B. P. A.; Broekaert, W. F. The complexity of disease signaling in Arabidopsis. Curr. Opin. Immunol. 13:63–68; 2001.

    Article  PubMed  CAS  Google Scholar 

  • Tian, D.; Araki, H.; Stahl, E.; Bergelson, J.; Kreitman, M. Signature of balancing selection in Arabidopsis. Proc. Natl Acad. Sci. USA 99:11525–11530; 2002.

    Article  PubMed  CAS  Google Scholar 

  • van der Biezen, E. A.; Jones, J. D. G. Plant disease resistance proteins and the ‘gene-for-gene’ concept. Trends Biochem. Sci. 23:454–456; 1998.

    Article  PubMed  Google Scholar 

  • Van der Hoorn, R. A.; de Wit, P. J.; Joosten, M. H. Balancing selection favors guarding resistance proteins. Trends Plant Sci. 7:67–71; 2002.

    Article  PubMed  Google Scholar 

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Correspondence to David Mackey.

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Mackey, D. SIVB 2003 Congress Symposium Proceeding: Plant-Targets of Pathogenic Effectors Can Transduce Both Virulence and Resistance Signals. In Vitro Cell.Dev.Biol.-Plant 40, 251–255 (2004). https://doi.org/10.1079/IVP2003523

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  • DOI: https://doi.org/10.1079/IVP2003523

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