Chapter 14 : Role of the Type III Protein Secretion System in Bacterial Infection of Plants

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Role of the Type III Protein Secretion System in Bacterial Infection of Plants, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815851/9781555814694_Chap14-1.gif /docserver/preview/fulltext/10.1128/9781555815851/9781555814694_Chap14-2.gif


In the past two decades, research into the molecular basis of bacterial pathogenesis has led to the conclusion that although different bacteria may use unique mechanisms to subvert hosts, a few strategies are common. One striking example is the discovery that many plant and animal bacterial pathogens contain members of a family of protein secretion systems classified as type III. The type III secretion system (TTSS) supramolecular structures in both mammalian and plant pathogenic bacteria have been characterized. The central importance of the TTSSs in mammalian and plant bacterial pathogenesis is underscored by the finding that a defect in this system often leads to a complete loss of bacterial pathogenicity. Plant pathogenic bacteria encounter a unique eukaryotic cell type that is enveloped by a cell wall; they multiply predominantly in the intercellular space outside of the plant cell wall and are therefore extracellular pathogen. Plant basal defense is associated with the induction of certain general defense genes, the production of antimicrobial phytoalexins, and the fortification of plant cell walls, which involves the localized deposition of callose (β-1,3-glucan) and other compounds in the plant cell wall. Recent studies show that certain virulent strains have found ways to break down gene-for-gene resistance and expand the host range at the cultivar level. TTSS effectors appear to be highly evolved microbial molecules that have adapted to carry out precise functions on specific host proteins.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Model for the activation and inactivation of basal defenses during subsp. DC3000 infection of susceptible plants. PAMPs from TTSS-defective mutants activate basal defense in an SA-independent manner. In the case of flagellin, perception is mediated by the FLS2 receptor, the signal is transduced via the MAPK3/6 pathway, and basal defense is activated ( ). In the ΔCEL mutant, the AvrPto class of effectors inactivates the SA-independent basal defense. However, the host cell partially overcomes the AvrPto-mediated inactivation of SA-independent basal defense and activates an SA-dependent basal defense pathway ( ). The bacterial factors involved in this SA-dependent activation are not known, but they may be type III effectors or the type III secretion process per se. In subsp. DC3000, HopM1 and AvrE inactivate the SA-dependent basal defense and promote disease-associated host cell death (necrosis). MAPKK, MAPK kinase; MAPKKK, MAPK kinase kinase. Plus and minus signs indicate degrees of effectiveness of host defense and bacterial virulence. Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Model for the virulence and avirulence functions of AvrRpt2, AvrRpm1, and RIN4 in In a susceptible plant (left), RIN4 negatively regulates basal defense (line 1), which is activated by PAMPs via the corresponding receptors (e.g., FLS2 for flagellin). The effector AvrRpm1 or AvrRpt2 is injected into an cell via the TTSS. The binding of AvrRpm1 to RIN4 induces RIN4 phosphorylation (P), which may augment the ability of RIN4 to suppress basal defense, via an unknown mechanism (line 2). AvrRpt2 cleaves RIN4. It is not known how the cleavage of RIN4 would enhance the suppressor function, unless the cleavage products are more potent as suppressors (line 3). AvrRpt2 targets multiple host proteins ( ), so its defense suppression function may be exerted via additional mechanisms ( ). In a resistant plant (right), besides its role in suppressing basal defense (data not shown), RIN4 is guarded by RPS2 and/or RPM1, which is in an inactive state ( ). The virulence action of AvrRpt2 (proteolysis) or AvrRpm1 (phosphorylation) on RIN4 activates the cognate resistance proteins and subsequent R protein-mediated resistance (arrows 4). In the presence of both AvrRpt2 and AvrRpm1, AvrRpm1/RPM1-dependent resistance is prevented because of the AvrRpt2-mediated removal of RIN4. At present, the molecular interplay between RIN4, Avr-Rpt2/Avr-Rpm1, and RPM1/RPS2 provides the most crucial evidence for the so-called guard hypothesis ( ), in which plant disease resistance proteins (e.g., RPM1 and RPS2) activate gene-for-gene resistance by monitoring host proteins (e.g., RIN4) that are targeted by cognate pathogen effector proteins (e.g., AvrRpm1 and AvrRPt2). Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

Schematic diagram depicting a putative polarized vesicle-trafficking pathway, in which AtMIN7 is a key component. The AtMIN7-dependent pathway is associated with localized plant immune responses, including the formation of callose deposits and probably the release of antimicrobial phytoalexins (dots in the papilla and plant cell wall) and cell wall thickening. DC3000 and presumably other strains inject HopM1 into the host cell ( ). Once inside the host cell, HopM1 is associated with an endomembrane compartment, binds to AtMIN7 through the N terminus, and promotes the ubiquitination and proteasome-dependent degradation of AtMIN7 and presumably other AtMIN proteins. BFA may mimic the effect of HopM1 by inhibiting the guanosine nucleotide exchange factor activity of the Sec7 protein family, of which AtMIN7 is a member. Golgi, Golgi apparatus; ER, endoplasmic reticulum; Ub, ubiquitin. Reprinted from ( ) with permission of the publisher.

Citation: He S. 2007. Role of the Type III Protein Secretion System in Bacterial Infection of Plants, p 209-220. In Brogden K, Minion F, Cornick N, Stanton T, Zhang Q, Nolan L, Wannemuehler M (ed), Virulence Mechanisms of Bacterial Pathogens, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815851.ch14
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abramovitch, R. B.,, Y. J. Kim,, S. Chen,, M. B. Dickman, and, G. B. Martin. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22: 6069.
2. Alfano, J. R.,, A. O. Charkowski,, W. L. Deng,, J. L Badel,, T. Petnicki-Ocwieja,, K. van Dijk, and, A. Collmer. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA 97: 48564861.
3. Arlat, M.,, F. V. Gijsegem,, J. C. Huet,, J. C. Pernollet, and, C. A. Boucher. 1994. PopA1, a protein which induces a hypersensitivity-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13: 543553.
4. Asai, T.,, G. Tena,, J. Plotnikova,, M. R. Willmann,, W. L. Chiu,, L. Gomez-Gomez,, T. Boller,, F. M. Ausubel, and, J. Sheen. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977983.
5. Axtell, M. J., and, B. J. Staskawicz. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369377.
6. Badel, J. L.,, K. Nomura,, S. Bandyopadhyay,, R. Shimizu,, A. Collmer, and, S. Y. He. 2003. Pseudomonas syringae pv. tomato DC3000 HopPtoM (CEL ORF3) is important for lesion formation but not growth in tomato and is secreted and translocated by the Hrp type III secretion system in a chaperone-dependent manner. Mol. Microbiol. 49: 12391251.
7. Badel, J. L.,, R. Shimizu,, H. S. Oh, and, A. Collmer. 2006. A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol. Plant-Microbe Interact. 19: 99111.
8. Beer, S. V.,, D. W. Bauer,, X. H. Jiang,, R. J. Laby,, B. J. Sneath,, Z. M. Wei,, D. A. Wilcox, and, C. H. Zumoff. 1991. The hrp gene cluster of Erwinia amylovora, p. 5360. In H. Hennecke and, D. P. S. Verma (ed.), Advances in Molecular Genetics of Plant Microbe Interactions. Kluwer Academic Publishers, Dordrecht, The Netherlands.
9. Belkhadir, Y.,, Z. Nimchuk,, D. A. Hubert,, D. Mackey, and, J. L. Dangl. 2004. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16: 28222835.
10. Bonas, U.,, R. Schulte,, S. Fenselau,, G. V. Minsavage,, B. J. Staskawicz, and, R. E. Stall. 1991. Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol. Plant-Microbe Interact. 4: 8188.
11. Boucher, C. A.,, F. Van Gijsegem,, P. A. Barberis,, M. Arlat, and, C. Zischek. 1987. Pseudomonas solanacearum genes controlling both pathogenicity on tomato and hypersensitivity on tobacco are clustered. J. Bacteriol. 169: 56265632.
12. Bretz, J. R.,, N. M. Mock,, J. C. Charity,, S. Zeyad,, C. J. Baker, and, S. W. Hutcheson. 2003. A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol. Microbiol. 49: 389400.
13. Brown, I.,, J. Mansfield, and, U. Bonas. 1995. hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papilla deposition in pepper mesophyll cells. Mol. Plant-Microbe Interact. 8: 825836.
14. Brown, I.,, J. Trethowan,, M. Kerry,, J. Mansfield, and, G. P. Bolwell. 1998. Localization of components of the oxidative cross-linking of glycoproteins and of callose synthesis in papillae formed during the interaction between nonpathogenic strains of Xanthomonas campestris and French bean mesophyll cells. Plant J. 15: 333343.
15. Buell, C. R.,, V. Joardar,, M. Lindeberg,, J. Selengut, and, I. T. Paulsen. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100: 1018110186.
16. Campellone, K. G., and, J. M. Leong. 2003. Tails of two Tirs: actin pedestal formation by enteropathogenic E. coli and enterohemorrhagic E. coli O157:H7. Curr. Opin. Microbiol. 6: 8290.
17. Celli, J.,, W. Deng, and, B. B. Finlay. 2000. Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell. Microbiol. 2: 19.
18. Chisholm, S. T.,, D. Dahlbeck,, N. Krishna-murthy,, B. Day,, K. Sjolander, and, B. J. Staskawicz. 2005. Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc. Natl. Acad. Sci. USA 102: 20872092.
19. Chisholm, S. T.,, G. Coaker,, B. Day, and, B. J. Staskawicz. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803814.
20. Coaker, G.,, A. Falick, and, B. Staskawicz. 2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308: 548550.
21. Coburn, J., and, D. W. Frank. 1999. Macrophages and epithelial cells respond differently to the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 67: 31513154.
22. Cornelis, G. R. 2002. The Yersinia Ysc-Yop ‘type III’ weaponry. Nat. Rev. Mol. Cell Biol. 3: 742752.
23. Cossart, P., and, P. J. Sansonetti. 2004. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304: 242248.
24. Dangl, J. L., and, J. D. G. Jones. 2001. Plant pathogens and integrated defense responses to infection. Nature 411: 826833.
25. Day, B.,, D. Dahlbeck,, J. Huang,, S. T. Chisholm,, D. Li, and, B. J. Staskawicz. 2005. Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell 17: 12921305.
26. DebRoy, S.,, R. Thilmony,, Y. B. Kwack,, K. Nomura, and, S. Y. He. 2004. A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in Arabidopsis. Proc. Natl. Acad. Sci. USA 101: 99279932.
27. Espinosa, A.,, M. Guo,, V. C. Tam,, Z. Q. Fu, and, J. R. Alfano. 2003. The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49: 377387.
28. Fang, F., and, A. Vazquez-Torres. 2002. Salmonella selectively stops traffic. Trends Microbiol. 10: 391392.
29. Fields, K. A.,, D. J. Mead,, C. A. Dooley, and, T. Hackstadt. 2003. Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol. Microbiol. 48: 671683.
30. Forsberg, A.,, I. Bolin,, L. Norlander, and, H. Wolf-Watz. 1987. Molecular cloning and expression of calcium-regulated, plasmid-coded proteins of Y. pseudotuberculosis. Microb. Pathog. 2: 123137.
31. Frank, D. W. 1997. The exoenzyme S regulon of Pseudomonas aeruginosa. Mol. Microbiol. 26: 621629.
32. Galan, J. E., and, R. I. Curtiss. 1989. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc. Natl. Acad. Sci. USA 86: 63836387.
33. Galan, J. E. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17: 5386.
34. Goguen, J. D.,, J. Yother, and, S. C. Straley. 1984. Genetic analysis of the low calcium response in Yersinia pestis Mu d1(Ap lac) insertion mutants. J. Bacteriol. 160: 842848.
35. Gomez-Gomez, L.,, G. Felix, and, T. Boller. 1999. A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18: 277284.
36. Gopalan, S.,, D. W. Bauer,, J. Alfano,, A. O. Loniello,, S. Y. He, and, A. Collmer. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8: 10951105.
37. Guttman, D. S.,, B. A. Vinatzer,, S. F. Sarkar,, M. V. Ranall,, G. Kettler, and, J. T. Greenberg. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 17221726.
38. Hauck, P.,, R. Thilmony, and, S. Y. He. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100: 85778582.
39. He, P.,, L. Shan,, N. C. Lin,, G. B. Martin,, B. Kemmerling,, T. Nurnberger, and, J. Sheen. 2006. Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563575.
40. He, S.,, H. Huang, and, A. Collmer. 1993. Pseudomonas syringae pv. syringae harpin Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73: 12551266.
41. He, S. Y. 1998. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36: 363392.
42. He, S. Y.,, K. Nomura, and, T. S. Whittam. 2004. Type III protein secretion mechanism in mammalian and plant pathogens. Biochim. Biophys. Acta 1694: 181206.
43. Heesemann, J.,, U. Gross,, N. Schmidt, and, R. Laufs. 1986. Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect. Immun. 54: 561567.
44. Jackson, R. W.,, E. Athanassopoulos,, G. Tsiamis,, J. W. Mansfield,, A. Sesma,, D. L. Arnold,, M. J. Gibbon,, J. Murillo,, J. D. Taylor, and, A. Vivian. 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: 1087510880.
45. Jakobek, J. L.,, J. A. Smith, and, P. B. Lindgren. 1993. Suppression of bean defense responses by Pseudomonas syringae. Plant Cell 5: 5763.
46. Jamir, Y.,, M. Guo,, H. S. Oh,, T. Petnicki Ocwieja,, S. Chen,, X. Tang,, M. B. Dickman,, A. Collmer, and, J. R. Alfano. 2004. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37: 554565.
47. Janjusevic, R.,, R. B. Abramovitch,, G. B. Martin, and, C. E. Stebbins. 2006. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311: 222226.
48. Jarvis, K. G.,, J. A. Giron,, A. E. Jerse,, T. K. McDaniel,, M. S. Donnenberg, and, J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA 92: 79968000.
49. Jia, J.,, M. Alaoui-El-Azher,, M. Chow,, T. C. Chambers,, H. Baker, and, S. Jin. 2003. c-Jun NH 2-terminal kinase-mediated signaling is essential for Pseudomonas aeruginosa ExoS-induced apoptosis. Infect. Immun. 71: 33613370.
50. Jin, P.,, M. D. Wood.,, Y. Wu,, Z. Xie, and, F. Katagiri. 2003. Cleavage of the Pseudomonas syringae type III effector AvrRpt2 requires a host factor[s] common among eukaryotes and is important for AvrRpt2 localization in the host cell. Plant Physiol. 133: 10721082.
51. Jin, Q. L., and, S. Y. He. 2001. Role of the Hrp pilus in type III secretion in Pseudomonas syringae. Science 294: 25562558.
52. Jin, Q. L.,, R. Thilmony,, J. Zwiesler-Vollick, and, S. Y. He. 2003. Type III secretion in Pseudomonas syringae. Microbes Infect. 5: 301310.
53. Juris, S. J.,, F. Shao, and, J. E. Dixon. 2002. Yersinia effectors target mammalian signalling pathways. Cell. Microbiol. 4: 201211.
54. Kalman, D.,, O. D. Weiner,, D. L. Goosney,, J. W. Sedat,, B. B. Finlay,, A. Abo, and, J. M. Bishop. 1999. Enteropathogenic E. coli acts through WASP and Arp2/3 complex to form actin pedestals. Nat. Cell Biol. 1: 389391.
55. Katagiri, F.,, R. Thilmony, and, S. Y. He. 27 March 2002, posting date. The Arabidopsis thaliana-Pseudomonas syringae interaction, p. 135. In C. R. Somerville and, E. M. Meyerowitz (ed.), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD. http://dx.doi.org/10.1199/tab.0039.
56. Kenny, B.,, R. DeVinney,, M. Stein,, D. J. Rein-scheid,, E. A. Frey, and, B. B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511520.
57. Kim, H. S.,, D. Desveaux,, A. U. Singer,, P. Patel,, J. Sondek, and, J. L. Dangl. 2005. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc. Natl. Acad. Sci. USA 102: 64966501.
58. Kim, M. G.,, L. D. Cunha,, A. J. McFall,, Y. Belkhadir,, S. DebRoy,, J. L. Dangl, and, D. Mackey. 2005. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121: 749759.
59. Knodler, L. A., and, O. Steele-Mortimer. 2005. The Salmonella effector PipB2 affects late endosome/lysosome distribution to mediate Sif extension. Mol. Biol. Cell 16: 41084123.
60. Kubori, T.,, Y. Matsushima,, D. Nakamura,, J. Uralil,, M. Lara-Tejero,, A. Sukhan,, J. E. Galan, and, S. I. Aizawa. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602605.
61. Leister, R. T.,, F. M. Ausubel, and, F. Katagiri. 1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc. Natl. Acad. Sci. USA 93: 1549715502.
62. Li, C. M.,, I. Brown,, J. Mansfield,, C. Stevens,, T. Boureau,, M. Romantschuk, and, S. Taira. 2002. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J. 21: 19091915.
63. Lindgren, P. B.,, R. C. Peet, and, N. J. Panopoulos. 1986. Gene cluster of Pseudomonas syringae pv. ‘ phaseolicola’ controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168: 512522.
64. Mackey, D.,, B. F. Holt,, A. Wiig, and, J. L. Dangl. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743754.
65. Mackey, D.,, Y. Belkhadir,, J. M. Alonso,, J. R. Ecker, and, J. L. Dangl. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379389.
66. Menard, R.,, C. Dehio, and, P. J. Sansonetti. 1996. Bacterial entry into epithelial cells: the paradigm of Shigella. Trends Microbiol. 4: 220226.
67. Miyata, S.,, M. Casey,, D. W. Frank,, F. M. Ausubel, and, E. Drenkard. 2003. Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71: 24042413.
68. Mossessova, E.,, R. A. Corpina, and, J. Goldberg. 2003. Crystal structure of ARF18*Sec7 complexed with brefeldin A and its implications for the guanine nucleotide exchange mechanism. Mol. Cell 12: 14031411.
69. Mudgett, M. B. 2005. New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu. Rev. Plant Biol. 56: 509531.
70. Mukherjee, S.,, G. Keitany,, Y. Li,, Y. Wang,, H. L. Ball,, E. J. Goldsmith, and, K. Orth. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 12111214.
71. Nomura, K.,, M. Melloto, and, S. Y. He. 2005. Suppression of host defense in compatible plant- Pseudomonas syringae interactions. Curr. Opin. Plant Biol. 8: 361368.
72. Nomura, K.,, S. Debroy,, Y. H. Lee,, N. Pumplin,, J. Jones, and, S. Y. He. 2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220223.
73. Petnicki-Ocwieja, T.,, D. J. Schneider,, V. C. Tam,, S. T. Chancey,, L. Shan,, Y. Jamir,, L. M. Schechter,, M. D. Janes,, C. R. Buell,, X. Tang,, A. Collmer, and, J. R. Alfano. 2002. Genome-wide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 99: 76527657.
74. Phillips, R. M.,, D. A. Six,, E. A. Dennis, and, P. Ghosh. 2003. In vivo phospholipase activity of the Pseudomonas aeruginosa cytotoxin ExoU and protection of mammalian cells with phospholipase A 2 inhibitors. J. Biol. Chem. 278: 4132641332.
75. Ritter, C., and, J. L. Dangl. 1996. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8: 251257.
76. Roine, E.,, W. Wei,, J. Yuan,, E. L. Nurmiaho Lassila,, N. Kalkkinen,, M. Romantschuk, and, S. Y. He. 1997. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 94: 34593464.
77. Rosqvist, R.,, K. Magnusson, and, H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13: 964972.
78. Salanoubat, M.,, S. Genin,, F. Artiguenave,, J. Gouzy,, S. Mangenot,, M. Arlat,, A. Billault,, P. Brottier,, J. C. Camus,, L. Cattolico,, M. Chandler,, N. Choisne,, C. Claudel-Renard,, S. Cunnac,, N. Demange,, C. Gaspin,, M. Lavie,, A. Moisan,, C. Robert,, W. Saurin,, T. Schiex,, P. Siguier,, P. Thebault,, M. Whalen,, P. Wincker,, M. Levy,, J. Weissenbach, and, C. A. Boucher. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497502.
79. Sanderfoot, A. A., and, N. V. Raikhel. 22 March 2003, posting date. The secretory system of Arabidopsis, p. 124. In C. R. Somerville and, E. M. Meyerowitz (ed.), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD. http://dx.doi.org/10.1199/tab.0098.
80. Sasakawa, C.,, K. Kamata,, T. Sakai,, S. Makino,, M. Yamada,, N. Okada, and, M. Yoshikawa. 1988. Virulence-associated genetic regions comprising 31 kilobases of the 230-kilobase plasmid in Shigella flexneri 2a. J. Bacteriol. 170: 24802484.
81. Sato, H.,, D. W. Frank,, C. J. Hillard,, J. B. Feix,, R. R. Pankhaniya,, K. Moriyama,, V. Finck Barbancon,, A. Buchaklian,, M. Lei,, R. M. Long,, J. Wiener-Kronish, and, T. Sawa. 2003. The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J. 22: 29592969.
82. Scofield, S. R.,, C. M. Tobias,, J. P. Rathjen,, J. H. Chang,, D. T. Lavelle,, R. W. Michelmore, and, B. J. Staskawicz. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274: 20632065.
83. Shotland, Y.,, H. Kramer, and, E. A. Groisman. 2003. The Salmonella SpiC protein targets the mammalian Hook3 protein function to alter cellular trafficking. Mol. Microbiol. 49: 15651576.
84. Simonet, M.,, S. Richard, and, P. Berch. 1992. Electron microscopic evidence for in vivo extracellular localization of Yersinia pseudotuberculosis harboring the pYV plasmid. Infect. Immun. 60: 366373.
85. Sory, M. P., and, G. R. Cornelis. 1994. Trans-location of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14: 583594.
86. Staskawicz, B. J.,, F. M. Ausubel,, B. J. Baker,, J. G. Ellis, and, J. D. Jones. 1995. Molecular genetics of plant disease resistance. Science 268: 661667.
87. Steinmann, T.,, N. Geldner,, M. Grebe,, S. Mangold,, C. L. Jackson,, S. Paris,, L. Galweiler,, K. Palme, and, G. Jurgens. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286: 316318.
88. Tang, X.,, R. D. Frederick,, J. Zhou,, D. A. Halterman,, Y. Jia, and, G. B. Martin. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274: 20602062.
89. Tran Van Nhieu, G.,, R. Bourdet-Sicard,, G. Dumenil,, A. Blocker, and, P. J. Sansonetti. 2000. Bacterial signals and cell responses during Shigella entry into epithelial cells. Cell. Microbiol. 2: 187193.
90. Tsiamis, G.,, J. W. Mansfield,, R. Hockenhull,, R. W. Jackson,, A. Sesma,, E. Athanassopoulos,, M. A. Bennett,, C. Stevens,, A. Vivian,, J. D. Taylor, and, J. Murillo. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19: 32043214.
91. Van den Ackerveken, G.,, E. Marois, and, U. Bonas. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 13071316.
92. Van der Biezen, E. A., and, J. D. G. Jones. 1998. Plant disease resistance proteins and the “gene-for-gene” concept. Trends Biochem. Sci. 23: 454456.
93. Waterman, S. R., and, D. W. Holden. 2003. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell. Microbiol. 5: 501511.
94. Wei, Z. M., and, S. V. Beer. 1993. HrpI of Erwinia amylovora functions in secretion of harpin and is a member of a new protein family. J. Bacteriol. 175: 79587967.
95. Yoshida, S., and, C. Sasakawa. 2003. Exploiting host microtubule dynamics: a new aspect of bacterial invasion. Trends Microbiol. 11: 139143.
96. Yoshida, S.,, E. Katayama,, A. Kuwae,, H. Mimuro,, T. Suzuki, and, C. Sasakawa. 2002. Shigella deliver an effector protein to trigger host microtubule destabilization, which promotes Rac1 activity and efficient bacterial internalization. EMBO J. 21: 29232935.
97. Zipfel, C.,, S. Robatzek,, L. Navarro,, E. J. Oakeley,, J. D. Jones,, G. Felix, and, T. Boller. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764767.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error