The hrpA and hrpC operons of Erwinia amylovora encode components of a type III pathway that secretes harpin

Journal of Bacteriology

Volumn 179, Issue 5, 1997, Pages 1690-1697

  Kim, Jihyun F ^a   Wei, Zhong Min ^a,b   Beer, Steven V ^a  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b Eden Bioscience Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENETICS; ERWINIA; NONHUMAN; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ERWINIA AMYLOVORA; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; RALSTONIA SOLANACEARUM; RHIZOBIUM; SHIGELLA FLEXNERI; SINORHIZOBIUM FREDII; XANTHOMONAS CAMPESTRIS; YERSINIA;

EID: 0031058133     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.5.1690-1697.1997     Document Type: Article

References (74)

1. Albertini, A. M., T. Caramori, W. D. Crabb, F. Scoffone, and A. Galizzi. 1991. The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide. J. Bacteriol. 173:3573-3579.
2. Allaoui, A., P. J. Sansonetti, and C. Parsot. 1993. MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri E. coli lpa invasins. Mol. Microbiol. 7:59-68.
3. Allaoui, A., P. J. Sansonetti, and C. Parsot. 1992. MxiJ, a lipoprotein involved in secretion of Shigella lpa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J. Bacteriol. 174:7661-7669.
4. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
5. Arlat, M., F. Van 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. 13:543-553.
6. Barny, M. A., M. H. Guinebretière, B. Marçais, E. Coissac, J. P. Paulin, and J. Laurent. 1990. Cloning of a large gene cluster involved in Erwinia amylovora CFBP 1430 virulence. Mol. Microbiol. 4:777-786.
7. Bauer, D. W. 1990. Molecular genetics of pathogenicity of Erwinia amylovora: techniques, tools and their application. Ph.D. thesis. Cornell University, Ithaca. N.Y.
8. Bauer, D. W., and S. V. Beer. 1991. Further characterization of an hrp gene cluster of Erwinia amylovora. Mol. Plant-Microbe Interact. 4:493-499.
9. Beck, E., and B. Zink. 1981. Nucleotide sequence and genome organisation of filamentous bacteriophage f1 and fd. Gene 16:35-58.
10. 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. 53-60. In H. Hennecke and D. P. S. Verma (ed.), Advances in molecular genetics of plant-microbe interactions. Kluwer Academic Publishers, Dordrecht, The Netherlands.
11. Beer, S. V., Z. M. Wei, B. Sneath, and J. F. Kim. Unpublished data.
12. Bergman, T., K. Erickson, E. Galyov, C. Persson, and H. Wolf-Watz. 1994. The lcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J. Bacteriol. 176:2619-2626.
13. 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.
14. Bogdanove, A. J., Z.-M. Wei, L. Zhao, and S. V. Beer. 1996. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of vopN of Yersinia. J. Bacteriol. 178:1720-1730.
15. Bonas, U. 1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79-98.
16. Boyd, D., and J. Beckwith. 1990. The role of charged amino acids in the localization of secreted and membrane proteins. Cell 62:1031-1033.
17. Braun, V., and H. C. Wu. 1994. Lipoproteins, structure, function, biosynthesis and model for protein export, p. 425-446. In J.-M. Ghuysen and R. Hakenbeck (ed.), Bacterial cell wall, vol. 27. Elsevier, New York.
18. Chou, P. Y., and G. D. Fasman. 1978. Prediction of the secondary structure of proteins from their amino acid sequence. Adv. Enzymol. 47:45-148.
19. Cornelis, G. R. 1994. Yersinia pathogenicity factors. Curr. Top. Microbiol. Immunol. 192:243-263.
20. d'Aubenton Carafa, Y., E. Brody, and C. Thermes. 1990. Prediction of rho-independent Escherichia coli terminators. A statistical analysis of their RNA stem-loop structures. J. Mol. Biol. 216:835-858.
21. d'Enfert, C., I. Reyss, C. Wandersman, and A. P. Pugsley. 1989. Protein secretion by gram-negative bacteria characterization of two membrane proteins required for pullulanase secretion by Escherichia coli K-12. J. Biol. Chem. 264:17462-17468.
22. Doolittle, R. F. 1986. Of URFs and ORFs: a primer on how to analyze derived amino acid sequences. University Science Books, Mill Valley, Calif
23. 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.
24. Fenselau, S., and U. Bonas. 1995. Sequence and expression analysis of the hrpB pathogenicity operon of Xanthomonas campestris pv. vesicatoria which encodes eight proteins with similarity to components of the Hrp, Ysc, Spa and Fli secretion systems. Mol. Plant-Microbe Interact. 8:845-854.
25. Galán, J. E. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
26. Gamier, J., D. J. Osguthorpe, and B. Robson. 1978. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 120:97-120.
27. 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.
28. 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.
29. He, S. Y. Personal communication.
30. He, S. Y., D. W. Bauer, A. Collmer, and S. V. Beer. 1994. Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabolism. Mol. Plant-Microbe Interact. 7:289-292.
31. Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266.
32. Huang, H.-C., S. Y. He, D. W. Bauer, and A. Collmer. 1992. The Pseudomonas syringae pv. syringae hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants. J. Bacteriol. 174:6878-6885.
33. Pss secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733-746.
34. 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.
35. Kaniga, K., J. C. Bossio, and J. E. Galan. 1994. The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins. Mol. Microbiol. 13:555-568.
36. Kihara, M., M. Homma, K. Kutsukake, and R. M. Macnab. 1989. Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences. J. Bacteriol. 171:3247-3257.
37. Klement, Z. 1982. Hypersensitivity, p. 149-177. In M. S. Mount and G. S. Lacy (ed.), Phytopathogenic prokaryotes. Academic Press, New York.
38. Laby, R. J., and S. V. Beer. 1992. Hybridization and functional complementation of the hrp gene cluster from Erwinia amylovora strain Ea321 and DNA of other bacteria. Mol. Plant-Microbe Interact. 5:412-419.
39. Pss secretion. Mol. Plant-Microbe Interact. 7:488-497.
40. Lindeberg, M., and A. Collmer. 1992. Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: sequence comparison with secretion genes from other gram-negative bacteria. J. Bacteriol. 174:7385-7397.
41. Lindgren, P. B., R. C. Peet, and N. J. Panopoulos. 1986. Gene cluster of Pseudomonas syringae pv. "phaseolicola'" controls pathogenieity of bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168:512-522.
42. Lonetto, M. A., K. L. Brown, K. E. Rudd, and M. J. Buttner. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. USA 91:7573-7577.
43. Manoil, C., and J. Beckwith. 1985. TnphoA: a transposon probe for protein export signals. Proc. Natl. Acad. Sci. USA 82:8129-8133.
44. Meinhardt, L. W., H. B. Krishnan, P. A. Balatti, and S. G. Pueppke. 1993. Molecular cloning and characterization of a sym plasmid locus that regulates cullivar-specific nodulation of soybean by Rhizobium fredii USDA257. Mol. Microbiol. 9:17-29.
45. 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.
46. Miller, J. F. 1994. Bacterial transformation by electroporation. Methods Enzymol. 235:375-385.
47. Parsot, C. 1994. Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells. Curr. Top. Microbiol. Immunol. 192:217-241.
48. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
49. Pegues, D. A., M. J. Hantmana, I. Behlau, and S. I. Miller. 1995. PhoP/EhoQ transcriptional repression of Salmonella typhimurium invasion genes: evidence for a role in protein secretion. Mol. Microbiol. 17:169-181.
50. Preston, G. M., 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.
51. Pugsley, A. P. 1993. The complete general secretory pathway in Gram- negative bacteria. Microbiol. Rev. 57:50-108.
52. Ramakrishnan, G., J. L. Zhao, and A. Newton. 1994. Multiple structural proteins are required for both transcriptional activation and negative auto-regulation of Caulobacter crescentus flagellar genes. J. Bacteriol. 176:7587-7600.
53. Rimpiläinen, M., Å. Forsberg, and H. Wolf-Watz. 1992. A novel protein LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH. J. Bacteriol. 174:3355-3363.
54. Russel, M. 1994. Phage assembly: a paradigm for bacterial virulence factor export? Science 265:612-614.
55. Russel, M., and B. Kazmierczak. 1993. Analysis of the structure and subcellular location of filamentous phage pIV. J. Bacteriol. 175:3998-4007.
56. 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.
57. Sambrook, J., E. F. Fritsch, and T. E. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
58. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
59. Shen, H., and N. T. Keen. 1993. Characterization of the promoter of avirulence gene D from Pseudomonas syringae pv. tomato. J. Bacteriol. 175:5916-5924.
60. Steinberger, E. M., and S. V. Beer. 1988. Creation and complementation of pathogenicity mutants of Erwinia amylovora. Mol. Plant-Microbe Interact. 1:135-144.
61. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 DNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
62. Tharaud, M., M. Menggad, J. P. Paulin, and J. Laurent. 1994. Virulence, growth, and surface characteristics of Erwinia amylovora mutants with altered pathogenicity. Microbiology 140:659-669.
63. 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.
64. van der Zwet, T., and S. V. Beer. 1995. Fire blight - its nature, prevention and control: a practical guide to integrated disease management. U.S. Department of Agriculture, Washington, D.C.
65. 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.
66. 1, vacuolar, and archaebacterial ATPase subunits. J. Bacteriol. 173:3564-3572.
67. Wattiau, P., S. Woestyn, and G. R. Cornells. 1996. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20:255-262.
68. Wei, Z.-M., and S. V. Beer. 1995. hrpL activates Erwinia amylovora hrp gene transcription and is a member of the ECF subfamily of CT factors. J. Bacteriol. 177:6201-6210.
69. 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. 175:7958-7967.
70. Wei, Z. M., R. J. Laby, C. H. Zumoff, D. W. Bauer, S. Y. He, A. Collmer, and S. V. Beer. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85-88.
71. Wei, Z. M., B. J. Sneath, and S. V. Beer. 1992. Expression of Erwinia amylovora hrp genes in response to environmental stimuli. J. Bacteriol. 174:1875-1882.
72. Willis, D. K., J. J. Rich, and E. M. Hrabak. 1991. hrp genes of phytopathogenic bacteria. Mol. Plant-Microbe Interact. 4:132-138.
73. Xiao, Y., and S. W. 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.
74. Zuberi, A. R., C. Ying, D. S. Bischoff, and G. W. Ordal. 1991. Gene-protein relationships in the flagellar hook-basal body complex of Bacillus subtilis sequences of the flgB,flgC,flgG, fliE, and fliF genes. Gene 101:23-32.