Skip to main content

Genomic Mining for Substrates of the Type III Secretion System of Pseudomonas syringae pv. tomato DC3000: New Insights into Mechanisms of Pathogenesis

  • Conference paper
Pseudomonas syringae and related pathogens

Abstract

The ability of Pseudomonas syringae pv. tomato DC3000 to be pathogenic on plants is dependent upon the type III secretion system (TTSS) and the effector proteins it translocates into plant cells. A draft sequence of DC3000 is currently being analysed for hop (Hrp outer protein) genes that encode TTSS substrates. Several different approaches were used to mine hop genes from the DC3000 genome. These approaches included ones that were based on linkage to other hop genes, the presence of apparent Hrp promoters, indicators of horizontal transfer, and N-terminal export-associated patterns. Many candidate hop genes were confirmed to encode TTSS-secreted proteins based on secretion and/or translocation assays. These approaches have substantially enlarged the inventory of DC3000 TTSS substrates. Hop proteins include extracellular accessory proteins that aid in translocation and effectors that are injected into plant cells. Several novel Hops have a clear potential to modify plant signal transduction pathways, which is consistent with the predicted roles for TTSS effectors. Activities of several Hops and new insights into bacterial pathogenesis of plants will be discussed.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abramovitch, R.B., Kim, Y.J., Chen, S., Dickman, M.B., and Martin, G.B., 2003, Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO 22: 60–69.

    CAS  Google Scholar 

  • Alfano, J.R., Kim, H.-S., Delaney, T.P., and Collmer, A., 1997, Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells. Mol. Plant-Microbe Interact. 10: 580–588.

    Article  PubMed  CAS  Google Scholar 

  • Alfano, J.R., Charkowski, A.O., Deng, W., Badel, J.L., Petnicki-Ocwieja, T., van Dijk, K., and Collmer, A., 2000, The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretions genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA 97: 4856–4861.

    Article  PubMed  CAS  Google Scholar 

  • Arnold, D.L., Gibbon, M.J., Jackson, R.W., Wood, J.R., Brown, J., Mansfield, J.W., Taylor, J.D., and Vivian, A., 2001, Molecular characterisation of avrPphD, a widely-distributed gene from Pseudomonas syringae pv. phaseolicola involved in non-host recognition by pea (Pisium sativum). Physiol. Mol. Plant Pathol. 58: 55–62.

    Article  CAS  Google Scholar 

  • Bennett, J.C., and Hughes, C., 2000, From flagellum assembly to virulence: The extended family of type III export chaperones. Trends Microbiol. 8: 202–204.

    Article  PubMed  CAS  Google Scholar 

  • Boyd, A.P., Lambermont, I., and Cornelis, G., 2000, Competition between the Yops of Yersinia enterocolitica for delivery in eukaryotic cells: Role of the SycE chaperone binding domain of YopE. J. Bacteriol. 182: 4811–4821.

    Article  PubMed  CAS  Google Scholar 

  • Charkowski, A.O., Alfano, J.R., Preston, G., Yuan, J., He, S.Y., and Collmer, A., 1998, The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J. Bacteriol. 180: 5211–5217.

    PubMed  CAS  Google Scholar 

  • Collmer, A., Lindeberg, M., Petnicki-Ocwieja, T., Schneider, D., and Alfano, J.R., 2002, Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10: 462–470.

    Article  PubMed  CAS  Google Scholar 

  • Cornelis, G., and van Gijsegem, F., 2000, Assembly and function of type III secretion systems. Annu. Rev. Microbiol. 54: 734–774.

    Article  Google Scholar 

  • Darwin, K.H., and Miller, V.L., 2001, Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO 20: 1850–1862.

    Article  CAS  Google Scholar 

  • Denu, J.M., Stuckey, J.A., Saper, M.A., and Dixon, J.E., 1996, Form and function in protein dephosphorylation. Cell 87: 361–364.

    Article  PubMed  CAS  Google Scholar 

  • Finlay, B.B., and Falkow, S., 1997, Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61: 136–169.

    PubMed  CAS  Google Scholar 

  • Fouts, D.E., Abramovitch, R.B., Alfano, J.R., Baldo, A.M., Buell, C.R., Cartinhour, S., Chatterjee, A.K., D’Ascenzo, M., Gwinn, M., Lazarowitz, S.G., Lin, N.-C., Martin, G.B., Rehm, A.H., Schneider, D.J., van Dijk, K., Tang, X., and Collmer, A., 2002, Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. USA 99: 2275–2280.

    Article  PubMed  CAS  Google Scholar 

  • Francis, M.S., Lloyd, S.A., and Wolf-Watz, H., 2001, The type III secretion chaperone LcrH co-operates with YopD to establish a negative, regulatory loop for control of Yop synthesis in Yersinia pseudotuberculosis. Mol. Microbiol. 42: 1075–1093.

    Article  CAS  Google Scholar 

  • Gaudriault, S., Malandrin, L., Paulin, J.-P., and Barny, M.-A., 1997DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol. Microbiol. 26: 1057–1069.

    Google Scholar 

  • Gaudriault, S., Paulin, J.-P., and Barny, M.-A., 2002, The DspB/F protein of Erwinina amylovora is a type III secretion chaperone ensuring efficient intrabacterial production of the Hrp-secreted DspA/E pathogenicity factor. Mol. Plant Pathol. 3:313–320.

    Google Scholar 

  • Guan, K.L., and Dixon, J.E., 1990, Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249: 553–556.

    Article  CAS  Google Scholar 

  • Guttman, D.S., Vinatzer, B.A., Sarkar, S.F., Ranall, M.V., Kettler, G., and Greenberg, J.T., 2002, A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722–1726.

    Article  CAS  Google Scholar 

  • Jackson, R.W., Athanassopoulos, E., Tsiamis, G., Mansfield, J.W., Sesma, A., Arnold, D.L., Gibbon, M.J., Murillo, J., Taylor, J.D., and Vivian, A., 1999, Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc. Natl. Acad. Sci. USA 96: 10875–10880.

    Article  PubMed  CAS  Google Scholar 

  • Lorang, J.M., and Keen, N.T., 1995, Characterization of avrE from Pseudomonas syringae pv. tomato: A hrp -linked avirulence locus consisting of at least two transcriptional units. Mol. Plant-Microbe Interact. 8: 49–57.

    Article  PubMed  CAS  Google Scholar 

  • Petnicki-Ocwieja, T., Schneider, D.J., Tam, V.C., Chancey, S.T., Shan, L., Jamir, Y., Schechter, L.M., Janes, M.D., Buell, C.R., Tang, X., Collmer, A., and Alfano, J.R., 2002, Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 99: 7652–7657.

    Article  PubMed  CAS  Google Scholar 

  • Plano, G.V., Day, J.B., and Ferracci, F., 2001, Type III export: new users for an old pathway. Mol. Microbiol. 40: 284–293.

    Article  PubMed  CAS  Google Scholar 

  • Tsiamis, G., Mansfield, J.W., Hockenhull, R., Jackson, R.W., Sesma, A., Athanassopoulos, E., Bennett, M.A., Stevens, C., Vivian, A., Taylor, J.D., and Murillo, J., 2000, Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO 19: 3204–3214.

    Article  CAS  Google Scholar 

  • Tucker, S.C., and Galan, J.E., 2000, Complex function for SicA, a Salmonella enterica serovar typhimurium type III associated chaperone. J. Bacteriol. 182: 2262–2268.

    Article  PubMed  CAS  Google Scholar 

  • van Dijk, K., Tam, V.C., Records, A.R., Petnicki-Ocwieja, T., and Alfano, J.R., 2002, The ShcA protein is a molecular chaperone that assists in the secretion of the HopPsyA effector from the type III (Hrp) protein secretion system of Pseudomonas syringae. Mol. Microbiol. 44: 1469–1481.

    Article  Google Scholar 

  • Wattiau, P., Woestyn, S., and Cornelis, G.R., 1996, Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20: 255–262.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, Z.Y., and Dixon, J.E., 1994, Protein tyrosine phosphatases: mechanism of catalysis and substrate specificity. Adv. Enzymol. Relat. Areas Mol. Biol. 68: 1–36.

    CAS  Google Scholar 

  • Zwiesler-Vollick, J., Plovanich-Jones, A.E., Nomura, K., Bandyopadhyay, S., Joardar, V., Kunkel, B.N., and He, S.Y., 2002, Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45: 1207–1218.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2003 Springer Science+Business Media Dordrecht

About this paper

Cite this paper

Alfano, J.R. et al. (2003). Genomic Mining for Substrates of the Type III Secretion System of Pseudomonas syringae pv. tomato DC3000: New Insights into Mechanisms of Pathogenesis. In: Iacobellis, N.S., et al. Pseudomonas syringae and related pathogens. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-0133-4_39

Download citation

  • DOI: https://doi.org/10.1007/978-94-017-0133-4_39

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-6267-3

  • Online ISBN: 978-94-017-0133-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics