The Pseudomonas syringae HopPtoV protein is secreted in culture and translocated into plant cells via the type III protein secretion system in a manner dependent on the ShcV type III chaperone

Journal of Bacteriology

Volumn 186, Issue 11, 2004, Pages 3621-3630

  Wehling, Misty D ^a,b   Guo, Ming ^a   Fu, Zheng Qing ^a   Alfano, James R ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NEBRASKA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVIRULENCE PROTEIN; AVR PROTEIN; BACTERIAL PROTEIN; CHAPERONE; DNA; HOPPTOV PROTEIN; HRP DEPENDENT OUTER PROTEIN; HYBRID PROTEIN; SHCV PROTEIN; UNCLASSIFIED DRUG;

ARABIDOPSIS; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BINDING SITE; CHROMOSOME; EFFECTOR GENE; GENOME; HRC GENE; HRP GENE; IMMUNOPRECIPITATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PLANT CELL; PLANT PATHOGEN INTERACTION; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; SACCHAROMYCES CEREVISIAE; TOMATO; TTC GENE;

BACTERIAL PROTEINS; BINDING SITES; MOLECULAR CHAPERONES; PLANTS; PROTEIN TRANSPORT; PSEUDOMONAS SYRINGAE; TWO-HYBRID SYSTEM TECHNIQUES;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 2442645221     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.11.3621-3630.2004     Document Type: Article

References (79)

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. 22:60-69.
2. Alfano, J. R., D. W. Bauer, T. M. Milos, and A. Collmer. 1996. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally nonpolar hrpZ deletion mutants, truncated HrpZ fragments, and hrmA mutations. Mol. Microbiol. 19:715-728.
3. Alfano, J. R., A. O. Charkowski, W. 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 97:4856-4861.
4. Alfano, J. R., and A. Collmer. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683-1698.
5. Alfano, J. R., and A. Collmer. 1997. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J. Bacteriol. 179:5655-5662.
6. 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 112:369-377.
7. Badel, J. L., A. O. Charkowski, W.-L. Deng, and A. Collmer. 2002. A gene in the Pseudomonas syringae pv. tomato Hrp pathogenicity island conserved effector locus, hopPtoA1, contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. Mol. Plant-Microbe Interact. 15:1014-1024.
8. 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. 49:1239-1251.
9. Bennett, J. C., and C. Hughes. 2000. From flagellum assembly to virulence: the extended family of type III export chaperones. Trends Microbiol. 8:202-204.
10. Birtalan, S., and P. Ghosh. 2001. Structure of the Yersinia type III secretory system chaperone SycE. Nat. Struct. Biol. 8:974-978.
11. Birtalan, S. C., R. M. Phillips, and P. Ghosh. 2002. Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol. Cell 9:971-980.
12. Bogdanove, A. J., J. F. Kim, Z. Wei, P. Kolchinsky, A. O. Charkowski, A. K. Conlin, A. Collmer, and S. V. Beer. 1998. Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc. Natl. Acad. Sci. USA 95:1325-1330.
13. Boyd, A. P., I. Lambermont, and G. Cornelis. 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.
14. Brent, R., and R. L. Finley, Jr. 1997. Understanding gene and allele function with two-hybrid methods. Annu. Rev. Genet. 31:663-704.
15. 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. 49:389-400.
16. Buell, C. R., V. Joardar, M. Lindeberg, S. J., I. T. Paulsen, M. L. Gwinn, R. J. Dodson, R. T. Deboy, A. S. Durkin, J. F. Kolonay, et al. 2003. The complete sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-10186.
17. Buttner, D., D. Nennstiel, B. Klusener, and U. Bonas. 2002. Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 184:2389-2398.
18. Cambronne, E. D., L. W. Cheng, and O. Schneewind. 2000. LcrQ/YscM1, regulators of the Yersinia yop virulon, are injected into host cells by a chaperone-dependent mechanism. Mol. Microbiol. 37:263-273.
19. Cambronne, E. D., and O. Schneewind. 2002. Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5′ untranslated region of yop mRNA. J. Bacteriol. 184:5880-5893.
20. Charkowski, A. O., H.-C. Huang, and A. Collmer. 1997. Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membranes of gram-negative bacteria. J. Bacteriol. 179:3866-3874.
21. Collmer, A., M. Lindeberg, T. Petnicki-Ocwieja, D. Schneider, and J. R. Alfano. 2002. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-469.
22. Cornelis, G., and F. van Gijsegem. 2000. Assembly and function of type III secretion systems. Annu. Rev. Microbiol. 54:734-774.
23. Cuppels, D. A. 1986. Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato. Appl. Environ. Microbiol. 51:323-327.
24. Dale, C., S. A. Young, D. T. Haydon, and S. C. Welburn. 2001. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc. Natl. Acad. Sci. USA 98:1883-1888.
25. Darwin, K. H., and V. L. Miller. 2001. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. EMBO J. 20:1850-1862.
26. Darwin, K. H., L. S. Robinson, and V. L. Miller. 2001. SigE is a chaperone for the Salmonella enterica serovar Typhimurium invasion protein SigD. J. Bacteriol. 183:1452-1454.
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. 49:377-387.
28. Evdokimov, A. G., J. E. Tropea, K. M. Routzahn, and D. S. Waugh. 2002. Three-dimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr. D 58:398-406.
29. Feldman, M. F., and G. R. Cornelis. 2003. The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol. Lett. 219:151-158.
30. Feldman, M. F., S. Muller, E. Wuest, and G. R. Cornelis. 2002. SycE allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol. Microbiol. 46:1183-1197.
31. Foultier, B., P. Troisfontaines, S. Muller, F. R. Opperdoes, and G. R. Cornelis. 2002. Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J. Mol. Evol. 55:37-51.
32. Fouts, D. E., R. B. Abramovitch, J. R. Alfano, A. M. Baldo, C. R. Buell, S. Cartinhour, A. K. Chatterjee, M. D'Ascenzo, M. Gwinn, S. G. Lazarowitz, N.-C. Lin, G. B. Martin, A. H. Rehm, D. J. Schneider, K. van Dijk, X. Tang, and A. Collmer. 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.
33. Francis, M. S., S. A. Lloyd, and H. Wolf-Watz. 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.
34. Galán, J. E., and A. Collmer. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328.
35. Gaudriault, S., J.-P. Paulin, and M.-A. Barny. 2002. The DspBfF 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.
36. Golemis, E. A., J. Gyuris, and R. Brent. 1994. Interaction trap/two-hybrid system to identify interacting proteins, p. 13.14.1-13.14.17. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates/John Wiley & Sons, New York, N.Y.
37. Greenberg, J. T., and B. A. Vinatzer. 2003. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6:20-28.
38. Guttman, D. S., and J. T. Greenberg. 2001. 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-Microbe Interact. 14:145-155.
39. 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 295:1722-1726.
40. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
41. 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 100:8577-8582.
42. Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266.
43. Hirano, S. S., and C. D. Upper. 2000. Bacterial in-the-leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64:624-653.
44. Huang, H.-C., R. Schuurink, T. P. Denny, M. M. Atkinston, C. J. Baker, I. Yucel, S. W. Hutcheson, and A. Collmer. 1988. Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J. Bacteriol. 170:4748-4756.
45. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
46. Huynh, T. V., D. Dahlbeck, and B. J. Staskawicz. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
47. Innes, R. W., A. F. Bent, B. N. Kunkel, S. R. Bisgrove, and B. J. Staskawicz. 1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175:4859-4869.
48. Jamir, Y., M. Guo, H.-S. Oh, T. Petnicki-Ocwieja, S. Chen, X. Tang, M. B. Dickman, A. Collmer, and J. R. Alfano. 2003. Identification of Pseudomonas syringae type III effectors that suppress programmed cell death in plants and yeast. Plant J. 37:554-565.
49. Kang, L., J. Li, T. Zhao, F. Xiao, X. Tang, R. Thilmony, S. He, and J. M. Zhou. 2003. Interplay of the Arabidopsis non host resistance gene NHO1 with bacterial virulence. Proc. Natl. Acad. Sci. USA 100:3519-3524.
50. Kelley, L. A., R. M. MacCallum, and M. J. Sternberg. 2000. Enhanced genome annotation using structural profiles in the program 3D-PSSM. J. Mol. Biol. 299:499-520.
51. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Med. 22:301-307.
52. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
53. Labes, M., A. Puhler, and R. Simon. 1990. A new family of RSF1010-derived expression and lac-fusion broad-host-range vectors for gram-negative bacteria. Gene 89:37-46.
54. 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. USA 98:289-294.
55. Lorang, J. L., H. Shen, D. Kobayashi, D. Cooksey, and N. T. Keen. 1994. avrA and avrE in Pseudomonas syringae pv. tomato play a role in virulence on tomato plants. Mol. Plant-Microbe Interact. 7:508-515.
56. Luo, Y., M. G. Bertero, E. A. Frey, R. A. Pfuetzner, M. R. Wenk, L. Creagh, S. L. Marcus, D. Lim, F. Sicheri, C. Kay, C. Haynes, B. B. Finlay, and N. C. Strynadka. 2001. Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat. Struct. Biol. 8:1031-1036.
57. 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 112:379-389.
58. Mavris, M., A. L. Page, R. Tournebize, B. Demers, P. Sansonetti, and C. Parsot. 2002. Regulation of transcription by the activity of the Shigella flexneri type III secretion apparatus. Mol. Microbiol. 43:1543-1553.
59. Mudgett, M. B., O. Chesnikova, D. Dahlbeck, E. T. Clark, O. Rossier, U. Bonas, and B. J. Staskawicz. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. USA 97:13324-13329.
60. Parsot, C., C. Hamiaux, and A. L. Page. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14.
61. 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. 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.
62. Ritter, C., and J. L. Dangl. 1995. The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. Plant-Microbe Interact. 8:444-453.
63. Rossler, O., G. Van den Ackerveken, and U. Bonas. 2000. HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol. Microbiol. 38:828-838.
64. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
65. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. Schechter, L. M., K. A. Roberts, Y. Jamir, J. R. Alfano, and A. Collmer. 2003. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol. 186:543-555.
67. Stebbins, C. E., and J. E. Galán. 2003. Priming virulence factors for delivery into the host. Nat. Rev. Mol. Cell. Biol. 4:738-743.
68. Stebbins, C. E., and J. E. Galán. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81.
69. Thomas, N. A., and B. B. Finlay. 2003. Establishing order for type III secretion substrates-a hierarchical process. Trends Microbiol. 11:398-403.
70. 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. 19:3204-3214.
71. van Dijk, K., D. E. Fouts, A. H. Rehm, A. R. Hill, A. Collmer, and J. R. Alfano. 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.
72. van Dijk, K., V. C. Tam, A. R. Records, T. Petnicki-Ocwieja, and J. R. Alfano. 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.
73. Vivian, A., and M. J. Gibbon. 1997. Avirulence genes in plant-pathogenic bacteria: signals or weapons. Microbiology 143:693-704.
74. Wattiau, P., and G. R. Cornelis. 1993. SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE. Mol. Microbiol. 8:123-131.
75. Wattiau, P., S. Woestyn, and G. R. Cornelis. 1996. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20:255-262.
76. Windgassen, M., A. Urban, and K.-E. Jaeger. 2000. Rapid gene inactivation in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 193:201-205.
77. Wulff-Strobel, C. R., A. W. Williams, and S. C. Straley. 2002. LcrQ and SycH function together at the Ysc type III secretion system in Yersinia pestis to impose a hierarchy of secretion. Mol. Microbiol. 43:411-423.
78. Yuan, J., and S. Y. He. 1996. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178:6399-6402.
79. Zwiesler-Vollick, J., A. E. Plovanich-Jones, K. Nomura, S. Bandyopadhyay, V. Joardar, B. N. Kunkel, and S. Y. He. 2002. Identification of novel hrpregulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45:1207-1218.