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

Journal of Bacteriology

Volumn 179, Issue 12, 1997, Pages 3866-3874

  Charkowski, Amy O ^a   Huang, Hsiou Chen ^b   Collmer, Alan ^a  

^a Cornell University ^*  (United States)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; CELL MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; PSEUDOMONAS SYRINGAE;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE PV. SYRINGAE; SALMONELLA; SHIGELLA; YERSINIA;

EID: 0030924763     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.12.3866-3874.1997     Document Type: Article

References (66)

1. Aizawa, S.-I. 1996. Flagellar assembly in Salmonella typhimurium. Mol. Microbiol. 19:1-5.
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 deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol. Microbiol. 19:715-728.
3. Allaoui, A., P. J. Sansonetti, and C. Parsot. 1992. MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J. Bacteriol. 174:7661-7669.
4. Allaoui, A., S. Woestyn, C. Sluiters, and G. R. Cornelis. 1994. YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion. J. Bacteriol. 176:4534-4542.
5. Arlat, M., F. Van Gijsegem, J. C. Huet, J. C. Pernollet, and C. A. Boucher. 1994. PopA1, a protein which induces a hypersensitive-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13:543-553.
6. Bischoff, D. S., and G. W. Ordal. 1992. Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex. Mol. Microbiol. 18:2715-2723.
7. Bogdanove, A. J., S. V. Beer, U. Bonas, C. A. Boucher, A. Collmer, D. L. Coplin, G. R. Cornelis, H.-C. Huang, S. W. Hutcheson, N. J. Panopoulos, and F. Van Gijsegem. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:681-683.
8. Bonas, U. 1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79-98.
9. Carpenter, P. B., A. R. Zuberi, and G. W. Ordal. 1943. Bacillus subtilis flagellar proteins FliP, FliQ, FliR and FlhB are related to Shigella flexneri virulence factors. Gene 137:243-245.
10. China, B., T. Michiels, and G. R. Cornelis. 1990. The pYV plasmid of Yersinia encodes a lipoprotein, YlpA, related to TraT. Mol. Microbiol. 4:1585-1593.
11. Collazo, C. M., M. K. Zierler, and J. E. Galan. 1995. Functional analysis of the Salmonella typhimurium invasion genes invI and invJ identification of a target of the protein secretion apparatus encoded in the inv locus. Mol. Microbiol. 15:25-38.
12. Dangl, J. L. 1994. The enigmatic avirulence genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:99-118.
13. 1 ATPase and to virulence proteins of mammalian and plant pathogens. J. Bacteriol. 175:3131-3138.
14. Fath, M. J., and R. Kolter. 1993. ABC transporters: bacterial exporters. Microbiol. Rev. 57:995-1017.
15. Fenselau, S., I. Balbo, and U. Bonas. 1992. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant-Microbe Interact. 5:390-396.
16. Forsberg, A., R. Rosqvist, and H. Wolf-Watz. 1994. Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol. 2:14-19.
17. Galan, J. E. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
18. Gopalan, S., D. W. Bauer, J. R. 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 8:1095-1105.
19. Gough, C. L., S. Genin, C. Zischek, and C. A. Boucher. 1992. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant-Microbe Interact. 5:384-389.
20. Groisman, E. A., and H. Ochman. 1993. Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J. 12:3779-3787.
21. Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266.
22. He, S. Y., M. Lindeberg, A. K. Chatterjee, and A. Collmer. 1991. Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc. Natl. Acad. Sci. USA 88:1079-1083.
23. Heu, S., and S. W. Hutcheson. 1993. Nucleotide sequence and properties of the hrmA locus associated with the Pseudomonas syringae pv. syringae 61 hrp gene cluster Mol. Plant-Microbe Interact. 6:553-564.
24. Huang, H.-C., S. Y. He, D. W. Bauer, and A. Collmer. 1992. The Pseudomonas syringae pv. syringae 61 hrpH product: an envelope protein required for elicitation of the hypersensitive response in plants. J. Bacteriol. 174:6878-6885.
25. Huang, H.-C., S. W. Hutcheson, and A. Collmer. 1991. Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning Hrp proteins. Mol. Plant-Microbe Interact. 4:469-476.
26. Pss secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733-746.
27. Huang, H.-C., R. Schuurink, T. P. Denny, M. M. Atkinson, 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 fluorescent to elicit the hypersensitive response in tobacco. J. Bacteriol. 170:4748-4756.
28. 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.
29. Kazmierczak, B. I., D. L. Mielke, M. Russel, and P. Model. 1994. pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer. J. Mol. Biol. 238:187-198.
30. Keen, N. T., S. Tamaki, D. Kobayashi, and D. Trollinger. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191-197.
31. 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.
32. Kutsukake, K., T. Minamino, and T. Yokoseki. 1994. Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J. Bacteriol. 176:7625-7629.
33. Leister, R. T., F. M. Ausubel, and K. 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 93:15497-15502.
34. Letoffe, S., P. Delepelaire, and C. Wandersman. 1990. Protease secretion by Erwinia chrysanthemi: the specific secretion functions are analogous to those of Escherichia coli alpha hemolysin. EMBO J. 9:1375-1382.
35. Pss secretion. Mol. Plant-Microbe Interact. 7:488-497.
36. 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. 168:512-522.
37. Macnab, R. M. 1996. Flagella and motility, p. 123-145. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella, vol. 1. ASM Press, Washington, D.C.
38. Malakooti, J., B. Ely, and P. Matsumura. 1994. Molecular characterization, nucleotide sequence, and expression of the fliO, fliP, fliQ, and fliR genes of Escherichia coli. J. Bacteriol. 176:189-197.
39. Menard, R., P. Sansonetti, C. Parsot, and T. Vasselon. 1994. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. flexneri. Cell 79:515-525.
40. Michiels, T., J.-C. Vanooteghem, C. L. de Rouvroit, B. China, A. Gustin, P. Boudry, and G. R. Cornelis. 1991. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J. Bacteriol. 173:4994-5009.
41. 2+ response. J. Bacteriol. 179:1307-1316.
42. Oosawa, K., T. Ueno, and S.-I. Aizawa. 1994. Overproduction of the bacterial flagellar switch proteins and their interactions with the MS ring complex in vitro. J. Bacteriol. 176:3683-3691.
43. Parsot, C., R. Menard, P. Gounon, and P. Sonsonetti. 1995. Enhanced secretion through the Shigella flexneri Mxi-Spa translocon leads to assembly of extracellular proteins into macromolecular structures. Mol. Microbiol. 16:291-300.
44. Pirhonen, M. U., M. C. Lidell, D. L. Rowley, S. W. Lee, S. Jin, Y. Liang, S. Silverstone, N. T. Keen, and S. W. Hutcheson. 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.
45. Plano, G. V., and S. C. Straley. 1995. Mutations in yscC, yscD, and yscG prevent high-level expression and secretion of V antigen and Yops in Yersinia pestis. J. Bacteriol. 177:3843-3854.
46. Prentki, P., and H. M. Krisch. 1984. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303-313.
47. Preston, G., H.-C. Huang, S. Y. He, and A. Collmer. 1995. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol. Plant-Microbe Interact. 8:717-732.
48. Pugsley, A. P. 1993. The complete general protein secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
49. Rosqvist, R., S. Hakansson, A. Forsberg, and H. Wolf-Watz. 1995. Functional conservation of the secretion and translocation machinery for virulence proteins of yersiniae, salmonellae and shigellae. EMBO J. 14:4187-4195.
50. Salmond, G. P. C., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. 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 274:2063-2065.
53. Shea, T. B. 1994. An inexpensive densitometric analysis system using a Macintosh™ computer and a desktop scanner. Biotechniques 16:1126-1128.
54. Staskawicz, B. J., F. M. Ausubel, B. J. Baker, J. G. Ellis, and D. G. Jones. 1995. Molecular genetics of plant disease resistance. Science 268:661-667.
55. Tang, H., and D. F. Blair. 1995. Regulated underexpression of the FliM protein of Escherichia coli and evidence for a location in the flagellar motor distinct from the MotA/MotB torque generators. J. Bacteriol. 177:3485-3496.
56. 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 274:2060-2062.
57. Ueno, T., K. Oosawa, and S.-I. Aizawa. 1994. Domain structures of the MS ring component protein (FliF) of the flagellar basal body of Salmonella typhimurium. J. Mol. Biol. 236:546-555.
58. Van den Ackerveken, G., E. Marois, and U. Bonas. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307-1316.
59. Van Gijsegem, F., S. Genin, and C. Boucher. 1993. Evolutionary conservation of pathogenicity determinants among plant and animal pathogenic bacteria. Trends Microbiol. 1:175-180.
60. Van Gijsegem, F., C. Gough, C. Zischek, E. Niqueux, M. Arlat, S. Genin, P. Barberis, S. German, P. Castello, and C. Boucher. 1995. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15:1095-1114
61. 1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173:3564-3572.
62. Wattiau, P., B. Bernier, P. Deslee, T. Michiels, and G. R. Cornelis. 1994 Individual chaperones required for Yop secretion by Yersinia. Proc. Natl. Acad. Sci. USA 91:10493-10497.
63. Witholt, B., M. Boekhout, M. Brock, J. Kingma, H. van Heerikhuizen, and L. deLeij. 1976. An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal. Biochem. 74:160-170.
64. Xiao, Y., S. Hue, J. Yi, Y. Lu, and S. W. Hutcheson. 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.
65. Xiao, Y., and S. Hutcheson. 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. (Author's correction, 176:6158.)
66. Yang, Y., and D. W. Gabriel. 1995. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol. Plant-Microbe Interact. 8:627-631.