Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulence functions by a HrpL-dependent promoter-trap assay

Molecular Plant-Microbe Interactions

Volumn 17, Issue 3, 2004, Pages 254-262

  Losada, L ^a   Sussan, T ^a   Pak, K ^a   Zeyad, S ^a   Rozenbaum, I ^a   Hutcheson, S W ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LYCOPERSICON ESCULENTUM; PHASEOLUS (ANGIOSPERM); PHASEOLUS VULGARIS; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 1642423868     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2004.17.3.254     Document Type: Article

References (61)

1. Abramovitch, R., Kim, Y.-J., Chen, S., Dickman, M., and Martin, G. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO (Eur. Mol. Biol. Organ.) J. 22:60-69.
2. Alfano, J. R., Charkowski, A. O., Deng, W.-L., Badel, J. L., PetnickiOcwieja, 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 secretion genes bound by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. U.S.A. 97:4856-4861.
3. Arnold, D., Gibbon, M., Jackson, R., Wood, J., Brown, J., Mansfield, J., Taylor, J., and Vivian, A. 2001. Molecular characterization of avrPphD, a widely distributed gene from Pseudomonas syringae pv. phaseolicola involved in non-host recognition by pea (Pisuin sativum). Physiol. Mol. Plant Pathol. 58:55-62.
4. Atlas, R. M. 1993. Handbook of Microbiological Media. CRC Press, Boca Raton, FL, U.S.A.
5. + exchange in tobacco. Phytopathology 77:1268-1272.
6. Bertoni, G., and Mills, D. 1987. A simple method to monitor growth of bacterial populations in leaf tissue. Phytopathology 77: 832-835.
7. Bretz, J., Mock, N., Charity, J., Zeyad, S., Baker, C., and Hutcheson, S. 2003. A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol. Microbiol. 49:389-400.
8. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
9. Charity, J., Pak, K., and Hutcheson, S. 2003. Novel exchangeable effector loci associated with the hrp pathogenicity island of P. syringae: Evidence for integron-like assembly from transposed gene cassettes. Mol. Plant-Microbe Interact. 16:495-507.
10. Chen, Z., Kloek, A. P., Boch, J., Katagiri, F., and Kunkel, B. N. 2000. The Pseudomonas syringae avrRpt2 gene product promotes pathogen virulence from inside plant cells. Mol. Plant-Microbe Interact. 13:1312-1321.
11. Collmer, A., Lindegerg, M., Petnicki-Ocwieja, T., Schneider, D., and Alfano, J. 2002. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-469.
12. Cornelis, G., and VanGijsegem, F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
13. Cuppels, D. A. 1986. Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl. Environ. Microbiol. 51:323-327.
14. Dangl, J., and Jones, J. 2001. Plant pathogens and integrated defence responses 10 infection. Nature (Lond.) 411:826-833.
15. Deng, W. L., Rehm, A., Charkowski, A., Rojas, C., and Collmer, A. 2003. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. svringae pv. syringae B728a. J. Bacteriol. 185:2592-2602.
16. Denny, T., Gilmour, M., and Selander, R. 1988. Genetic diversity and relationships of two pathovars of Pseudomonas syringae. J. Gen. Microbiol. 134:1949-1960.
17. Espinosa, A., Guo, M., Tam, V., Fu, Z., and Alfano, J. 2003. The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49:377-387.
18. Fouts, D., Abramovitch, R., Alfano, J., Baldo, A., Buell, C., Cartinhour, S., Chatterjee, A., D'Ascenzo, M., Gwinn, M., Lazarowitz, S., Lin, N.-C., Martin, G., Rehm, A., Schneider, D., vanDijk, 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.
19. Gopalan, S., Bauer, D. W., Alfano, J. R., Loniello, A. O., He, S. Y., and Collmer, A. 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 8:1095-1105.
20. Greenberg, J., and Vinatzer, B. 2003. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6:20-28.
21. Guttman, D., Vinatzer, B., Sarkar, S., Ranall, M., Kettler, G., and Greenberg. J. 2002. A functional screen for the type III secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-1726.
22. Huang, H. C., Hutcheson, S. W., and Collmer, A. 1991. Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of exported or membrane-spanning Hrp proteins. Mol. Plant-Microbe Interact. 4:469-476.
23. Hutcheson, S. 2001. The molecular biology of hypersensitivity to plant pathogenic bacteria. J. Plant Pathol. 83:151-172.
24. Hutcheson, S. W. 1999. The hrp cluster of Pseudomonas syringae: a pathogenicity island encoding a type 111 protein translocation complex? Pages 309-329 in: Pathogenicity Islands and Other Mobile Virulence Elements. J. B. Kaper and J. Harker, eds. American Society of Microbiology, Washington, D.C..
25. Hutcheson, S. W., Bretz, J., Sussan, T., Jin, S., and Pak, K. 2001. The enhancer binding protein HrpR and HrpS interact to regulate hrp-encoded type III protein secretion in Pseudomonas syringae strains. J. Bacteriol. 183:5589-5598.
26. Innes, N., Conway, J., and Taylor, J. 1984. Resistance to halo-blight in the Cambridge accessions V4604 and V4058 of Phaseolus beans. Ann. Appl. Biol. 104:307-314.
27. Jackson, R. W., Athanassopoulos, E., Tsiamis, G., Mansfield, J. W., Sema, 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 pv. phaseolicola. Proc. Natl. Acad. Sci. U.S.A. 96:10875-10880.
28. Keen, N., Tamaki, J., Kobayashi, D., and Trollinger, D. 1988. Improved broad host range plasmids for DNA cloning in gram negative bacteria. Gene 70:191-197.
29. Kim, J. F., Charkowski, A. O., Alfano, J. R., Collmer, A., and Beer, S. V. 1998. Sequences related to transposable elements and bacteriophages flank avirulence genes of Pseudomonas syringae. Mol. Plant-Microbe Interact. 11:1247-1252.
30. Leach, J. E., and White, F. F. 1996. Bacterial avirulence genes. Annu. Rev. Phytopathol. 34:153-179.
31. Psph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. Proc. Natl. Acad. Sci. U.S.A. 98:289-294.
32. Leister, R. T., Ausubel, F. M., and Katagiri, F. 1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and KPM1. Proc. Natl. Acad. Sci. U.S.A. 93:3459-3464.
33. Lindgren, P. B., Peet, R. C., and Panopoulos, N. J. 1986. Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity on bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168:512-522.
34. Liu, Y., and Whittier, R. 1995. Thermal asymmetric interlaced PCR: Automatable amplification and sequencing of insert end fragments from PI and YAC clones for chromosome walking. Genomics 25:674-681.
35. 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.
36. Mackey, D., Holt, B., Wiig, A., and Dangl. J. 2002. R1N4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-754.
37. Mayer, M. P 1995. A new set of useful cloning and expression vectors derived from pBluescript. Gene 163:41-46.
38. Menard, R., Sansonetti, P. J., and Parsot, C. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5965.
39. Miller, J. H. 1971. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. 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.
41. Ochman, H., Medhora, M. M., Garza, D., and Hartle, D. L. 1990. Amplification of flanking sequences by inverse PCR., p. 219-227. In: T. J. White (ed.), PCR protocols, a guide to methods and applications. Academic Press Inc., London.
42. Petnicki-Ocweija, T., Schneider, D., Tam, V., Chancey, S., Shan, L., Jamir, Y., Schechter, L., Janes, M., Buell, C., Tang, X., Collmer, A., and Alfano, J. 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.
43. Pirhonen, M. U., Lidell, M. C., Rowley, D., Lee, S. W., Silverstone, S., Liang, Y., Keen, N. T., and Hutcheson, S. W. 1996. Phenotypic expression of Pseudomonas syringae avr genes in E. coli is linked to the activities of the hrp-encoded secretion system. Mol. Plant-Microbe Interact. 9:252-260.
44. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
45. Sawada, H., Suzuki, F., Matsuda, I., and Saitou. N. 1999. Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. J. Mol. Evol. 49:627-644.
46. 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 2074:2063-2065.
47. Shao, F., Merritt, P., Bao, Z., Innes, R., and Dixon, J. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-588.
48. Shapiro, A., and Zhang, C. 2001. The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol. 127:1089-1101.
49. Silhavy, T. J., Bernman, M. L., and Enquist, L. W. 1984. Experiments with Gene Fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
50. Staskawicz, B. J., Dahlbeck, D., and Keen, N. T. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc. Nail. Acad. Sci. U.S.A. 81:6024-6028.
51. Staskawicz, B. J., Dahlbeck, D., Keen, N., and Napoli, C. 1987. Molecular characterization of cloned avirulence genes from race O and 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
52. Stevens, C., Bennett, M., Athanossopoulos, E., Tsiamis, G., Taylor, J., and Mansfield, J. 1998. Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Mol. Microbiol. 29:165-177.
53. 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.
54. Tsiamis, G., Mansfield, J., Hockenhull, R., Jackson, R., Sesma, A., Athanassopoulos, E., Bennett, M., Stevens, C., Vivian, A., Taylor, J., 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.
55. Van den Eede, G., Deblaere, R., Goethals, K., Van Montagu, M., and Holsters, M. 1992. Broad host range and promoter selection vectors for bacteria that interact with plants. Mol. Plant-Microbe Interact. 5:228-234.
56. Vivian, A., and Gibbon, M. J. 1997. Avirulence genes in plant-pathogenic bacteria: signals or weapons. Microbiology 143:693-704.
57. 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 111 secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc. Natl. Acad. Sci. U.S.A. 97:2247-2252.
58. Xiao, Y., Heu, S., Yi, J., Lu, Y., and Hutcheson, S. W. 1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J. Bacteriol. 176:1025-1036.
59. Xiao, Y., and Hutcheson, S. W. 1994. A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. J. Bacteriol. 176:3089-3091.
60. Yuan, J., and He, S. Y. 1996. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178:6399-6402.
61. Zwiesler-Vollick, J., Plovanich, J., Nomura, K., Bandyopadhyay, S., Joardar, V., Kundel, B., and He, S. 2002. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45:1207-1218.