The HopPtoF Locus of Pseudomonas syringae pv. tomato DC3000 encodes a type III chaperone and a cognate effector

Molecular Plant-Microbe Interactions

Volumn 17, Issue 5, 2004, Pages 447-455

  Shan, Libo ^a,d   Oh, Hye Sook ^b   Chen, Jianfu ^a   Guo, Ming ^c   Zhou, Jianmin ^a   Alfano, James R ^c   Collmer, Alan ^b   Jia, Xu ^d   Tang, Xiaoyan ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; NEGIBACTERIA; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. PHASEOLICOLA; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 1942504720     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2004.17.5.447     Document Type: Article

References (46)

1. Aldridge, P., and Hughes, K. T. 2001. How and when are substrates selected for type III secretion? Trends Microbiol. 9:209-214.
2. Badel, J. L., Nomura, K., Bandyopadhyay, S., Shimizu, R., Collmer, A., and He, S. Y. 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. 49:1239-1251.
3. Bennett, J. C. Q., and Hughes, C. 2000. From flagellum assembly to virulence: The extended family of type III export chaperones. Trends Microbiol. 8:202-204.
4. 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 265:1856-60.
5. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q., Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W. L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186.
6. Cambronne, E. D., Cheng, L. W., and Schneewind, O. 2000. LcrQ/YscM1, regulators of the Yersinia yop virulon, are injected into host cells by a chaperone-dependent mechanism. Mol. Microbiol. 37:263-73.
7. Collmer, A. 1998. Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr. Opin. Plant Biol. 1:329-335.
8. Collmer, A., Lindeberg, M., Petnicki-Ocwieja, T., Schneider, D., and Alfano, J. 2002. Genomic mining type in secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-467.
9. Deng, W. L., Rehm, A. H., Charkowski, A. O., Rojas, C. M., and Collmer, A. 2003. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J. Bacteriol. 185:2592-2602.
10. 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. L., 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. U.S.A. 99:2275-2280.
11. Fu, Y., and Galan, J. E. 1998. Identification of a specific chaperone for SptP, a substrate of the centisome 63 type III secretion system of Salmonella typhimurium. J. Bacteriol. 180:3393-3399.
12. Galan, J. E., and Collmer, A. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
13. Gaudriault, S., Paulin, J.-P., and Barny, M.-A. 2002. The DspB/F protein of Erwinia 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.
14. Golemis, E. A., Serebriiskii, I., Gyuris, J., and Brent, R. 1997. Interaction trap/two-hybrid system to identify interacting proteins. Pages 20.1.1-20.1.35 in: Current Protocols in Molecular Biology. F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl, eds. Greene Publishing Associates/John Wiley and Sons, New York.
15. Guan, K. L., and Dixon, J. E. 1991. Eukaryotic proteins expressed in Escherichia coli: An improved thrombin cleavage and purification of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262-267.
16. Guttman, D. S, and Greenberg, J. T. 2001. Functional analysis of the type HI effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant-Microbe Interact. 14:145-155.
17. 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.
18. He, S. Y. 1998. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36:363-392.
19. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
20. Huynh, T. V., Dahlbeck, D., and Staskawicz, B. J. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
21. 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. U.S.A. 96:10875-10880.
22. Kim, Y. J., Lin, N. C., and Martin, G. B. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589-98.
23. King, E. O., Ward, M. K., and Raney, D. E. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Med. 22:301-307.
24. Lindgren, P. B. 1997. The role of hrp genes during plant-bacterial interactions. Annu. Rev. Phytopathol. 35:129-152.
25. Mackey, D., Holt, B. F, Wiig, A., and Dangl, J. L. 2002. RIN4 interacts with Pseudomonas syringae type in effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-754.
26. McGuffin, L. J., Bryson, K., and Jones, D. T. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
27. Mudgett, M. B, Chesnokova, O., Dahlbeck, D., Clark, E. T, Rossier, O., Bonas, U., and Staskawicz, B. J. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. U.S.A. 97:13324-13329.
28. Mudgett, M. B, and Staskawicz, B. J. 1999. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol. Microbiol. 32:927-941.
29. Niebuhr, K., Jouihri, N., Allaoui, A., Gounon, P., Sansonetti, P. J., Parsot, C. 2000. IpgD, a protein secreted by the type III secretion machinery of Shigella flexneri, is chaperoned by IpgE and implicated in entry focus formation. Mol. Microbiol. 38:8-19.
30. Osawa, S., Jukes, T. H., Watanabe, K., and Muto, A. 1992. Recent evidence for evolution of the genetic code. Microbiol. Rev. 56:229-264.
31. Page, A. L., and Parsot, C. 2002. Chaperones of the type III secretion pathway: jacks of all trades. Mol. Microbiol. 46:1-11.
32. Parsot, C., Hamiaux, C., and Page, A. L. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14.
33. 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. U.S.A. 99:7652-7657.
34. Ronald, P. C., Salmeron, J. M., Carland, F. M., and Staskawicz, B. J. 1992. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174:1604-1611.
35. Salzberg, S. L., Delcher, A. L., Kasif, S., and White, O. 1998. Microbial gene identification using interpolated Markov models. Nucleic Acids Res. 26:544-548.
36. Scofield, S. R., Tobias, C. M., Rathjen, J. P., Chang, J. H., Lavelle, D. T., Michelmore, R. W., and Staskawicz, B. J. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063-2065.
37. Shan, L., Thara, V. K., Martin, G. B., Zhou, J. M., and Tang, X. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323-2338.
38. Shao, F., Golstein, C., Ade, J., Stoutemyer, M., Dixon, J. E., and Innes, R. W. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230-1233.
39. Tang, X., Frederick, R. D., Zhou, J., Halterman, D. A., Jia, Y., and Martin, G. B. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2063.
40. 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 (Eur. Mol. Biol. Organ.) J. 19:3204-3214.
41. van Dijk, K., Fouts, D. E., Rehm, A. H., Hill, A. R., Collmer, A., and Alfano, J. R. 1999. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature-and pH-sensitive manner. J. Bacteriol. 181:4790-4797.
42. van Dijk, K., Tam, V. C., Records, A. R., Petnicki-Ocwieia, 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.
43. Wei, W., Plovanich-Jones, A., Deng, W. L., Jin, Q. L., Collmer, A., Huang, H. C., and He, S.-Y. 2000. The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc. Natl. Acad. Sci. U.S.A. 97:2247-2252.
44. White, F. F., Yang, B., and Johnson, L. B. 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3:291-298.
45. Zhu, W., Yang, B., Chittoor, J. M., Johnson, L. B., and White, F. F. 1998. AvrXalO contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol. Plant-Microbe Interact. 11:824-832.
46. 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.