hpaA mutants of Xanthomonas campestris pv. vesicatoria are affected in pathogenicity but retain the ability to induce host-specific hypersensitive reaction

Molecular Microbiology

Volumn 29, Issue 6, 1998, Pages 1379-1390

  Huguet, Elisabeth ^a   Hahn, Karoline ^a   Wengelnik, Kai ^a,b   Bonas, Ulla ^a,c  

^a CNRS   (France)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SIGNAL PEPTIDE;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM COMPETENCE; BACTERIUM MUTANT; CHROMOSOME MAP; DNA SEQUENCE; GENE CLUSTER; GENE CONTROL; HOST SUSCEPTIBILITY; NONHUMAN; PEPPER; PHYTOTOXICITY; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL DETECTION; SITE DIRECTED MUTAGENESIS; SUICIDE GENE; TOMATO; XANTHOMONAS CAMPESTRIS;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CAPSICUM; DNA PRIMERS; DNA, BACTERIAL; GENES, BACTERIAL; HEMAGGLUTININS; LECTINS; LIPOPROTEINS; LYCOPERSICON ESCULENTUM; MAMMALS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR LOCALIZATION SIGNALS; OPERON; PHENOTYPE; PLANT DISEASES; PLANTS, MEDICINAL; VIRULENCE; XANTHOMONAS CAMPESTRIS;

ANIMALIA; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; MAMMALIA; NEGIBACTERIA; RALSTONIA SOLANACEARUM; XANTHOMONAS; XANTHOMONAS CAMPESTRIS PV. VESICATORIA;

EID: 0031671381     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.01019.x     Document Type: Article

References (74)

1. Aiba, H., Adhya, S., and de Crombugghe, B. (1981) Evidence of two functional gal promoters in intact Escherichia coli cells. J Biol Chem 256: 11905-11910.
2. Alfano, J.R., and Collmer, A. (1996) Bacterial pathogens in plants: life up against the wall. Plant Cell 8: 1683-1698.
3. Alfano, J.R., and Collmer, A. (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179: 5655-5662.
4. Altschul, S.F., Gish, W., Miller, W., Meyers, E., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Arlat, M., Van Gijsegem, F., Huet, J.C., Pernollet, J.C., and Boucher, C.A. (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. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., et al. (1996) Current Protocols in Molecular Biology. New York: John Wiley & Sons.
7. Barny, M.A., Guinebretière, M.H., Marçais, B., Coissac, E., Paulin, J.P., and Laurent, J. (1990) Cloning of a large gene cluster involved in Erwinia amylovora CFBP1430 virulence. Mol Microbiol 4: 777-786.
8. Bauer, D.W., Bogdanove, A.J., Beer, S.V., and Collmer, A. (1994) Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol Plant-Microbe Interact 7: 573-581.
9. Bergman, T., Erickson, K., Galyov, E., Persson, C., and WolfWatz, H. (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.
10. Bischoff, D.S., and Ordal, G.W. (1992) Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex. Mol Microbiol 6: 2715-2723.
11. Bischoff, D.S., Weinreich, M.D., and Ordal, G.W. (1992) Nucleotide sequences of Bacillus subtilis flagellar biosynthetic genes fliP and fliQ and identification of a novel flagellar gene, fliZ. J Bacteriol 174: 4017-4025.
12. Bogdanove, A., Beer, S.V., Bonas, U., Boucher, C.A., Collmer, A., Coplin, D.L., et al. (1996a) Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol Microbiol 20: 681-683.
13. Bogdanove, A.J., Wei, Z.M., Zhao, L., and Beer, S.V. (1996b) Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopNol Yersinia spp. J Bacteriol 178: 1720-1730.
14. Bonas, U. (1994) hrp genes of phytopathogenic bacteria. Curr Topics Microbiol Immunol 192: 79-98.
15. Bonas, U., and Van den Ackerveken, G. (1997) Recognition of bacterial avirulence proteins occurs inside the plant cell: a general phenomenon in resistance to bacterial diseases. Plant J 12: 1-7.
16. Bonas, U., Stall, R.E., and Staskawicz, B. (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet 218: 127-136.
17. Bonas, U., Schulte, R., Fenselau, S., Minsavage, G.V., and Staskawicz, B.J. (1991) Isolation of a gene cluster from Xanthomonas campestris pv. vesicatoria that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol Plant-Microbe Interact 4: 81-88.
18. Bonas, U., Conrads-Strauch, J., and Baltao, I. (1993) Resistance in tomato to Xanthomonas campestris pv vesicatoria is determined by alleles of the pepper-specific avirulence gene avrBs3. Mol Gen Genet 238: 261-269.
19. Brown, I., Mansfield, J., and Bonas, U. (1995) hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papillae deposition in pepper mesophyll cells. Mol Plant-Microbe Interact 8: 825-836.
20. Citovsky, V., Zupan, J., Warnick, D., and Zambryski, P. (1992) Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256: 1802-1805.
21. Collazo, C.M., and Galan, J.E. (1996) Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect Immun 64: 3524-3531.
22. Cornells, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
23. Daniels, M.J., Barber, C.E., Turner, P.C., Sawczyc, M.K., Byrde, R.J.W., and Fielding, A.M. (1984) Cloning of genes involved in pathogenicity of Xanthomonas campestris pv. campestris using the broad host range cosmid pLAFR1. EMBO J 3: 3323-3328.
24. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. (1980) Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77: 7347-7351.
25. Fan, F., Ohnishi, K., Francis, N.R., and Macnab, R.M. (1997) The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Mol Microbiol 26: 1035-1046.
26. Fenselau, S., and Bonas, U. (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.
27. Fenselau, S., Balbo, I., and Bonas, U. (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.
28. 2+ response (LCR) secretion (ysc) locus lies within the lcrB region of the LCR plasmid in Yersinia pestis. J Bacteriol 176: 569-579.
29. Figurski, D., and Helinski, D.R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 76: 1648-1652.
30. Freiberg, C., Fellay, R., Bairoch, A., Broughton, W.J., Rosenthal, A., and Perret, X. (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394-401.
31. Galan, J.E. (1996) Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol 20: 263-271.
32. Gaudriault, S., Malandrin, L., Paulin, J.-P., and Barny, M.-A. (1997) DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol 26: 1057-1069.
33. Gober, J.W., Boyd, C.H., Jarvis, M., Mangan, E.K., Rizzo, M.F., and Wingrove, J.A. (1995) Temporal and spatial regulation of fliP, an early flagellar gene of Caulobacter crescentus that is required for motility and normal cell division. J Bacteriol 177: 3656-3667.
34. Groisman, E.A., and Ochman, H. (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J 12: 3779-3787.
35. He, S.Y. (1997) Hrp-controlled interkingdom protein transport: learning from flagellar assembly? Trends Microbiol 5: 489-495.
36. He, S.Y., Huang, H.C., and Collmer, A. (1993) Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73: 1255-1266.
37. Howard, E.A., Zupan, J.R., Citovsky, V., and Zambryski, P.C. (1992) The VirD2 protein of A. tumefaciens contains a C-terminal bipartite nuclear localization signal: implications for nuclear uptake of DNA in plant cells. Cell 68: 109-118.
38. Huang, H.C., Lin, R.H., Chang, C.J., Collmer, A., and Deng, W.L. (1995) The complete hrp gene cluster of Pseudomonas syringae pv. syringae 61 includes two blocks of genes required for harpinPss secretion that are arranged collinearly with Yersinia ysc homologs. Mol Plant-Microbe Interact 8: 733-746.
39. Huguet, E., and Bonas, U. (1997) hrpF of Xanthomonas campestris pv. vesicatoria encodes an 87-kDa protein with homology to NoIX of Rhizobium fredii. Mol Plant-Microbe Interact 10: 488-498.
40. Kaniga, K., Delor, I., and Cornells, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109: 137-141.
41. Keen, N.T., and Tamaki, S. (1986) Structure of two pectate lyase genes from Erwinia chrysanthemi EC16 and their high-level expression in Escherichia coli. J Bacteriol 168: 595-606.
42. Knoop, V., Staskawicz, B., and Bonas, U. (1991) Expression of the avirulence gene avrBs3 frorn Xanthomonas campestris pv. vesicatoria is not under the control of hrp genes and is independent of plant factors. J Bacteriol 173: 7142-7150.
43. Kubori, T., Yamaguchi, S., and Aizawa, S.-I. (1997) Assembly of the switch complex onto the MS ring complex of Salmonella typhimurium does not require any other flagellar proteins. J Bacteriol 179: 813-817.
44. Li, J., Ochman, H., Groisman, E.A., Boyd, E.F., Solomon, F., Nelson, K., et al. (1995) Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci USA 92: 7252-7256.
45. Lidell, M.C., and Hutcheson, S.W. (1994) Characterization of the hrpJ and hrpU operons of Pseudomonas syringae pv. syringae Pss61: similarity with components of enteric bacteria involved in flagellar biogenesis and demonstration of their role in harpinPss secretion. Mol Plant-Microbe Interact 7: 488-497.
46. Malakooti, J., Ely, B., and Matsumura, P. (1994) Molecular characterization, nucleotide sequence, and expression of the fliO, fliQ, and fliR genes of Escherichia coli. J Bacteriol 176: 189-197.
47. Meinhardt, L.W., Krishnan, H.B., Balatti, P.A., and Pueppke, S.G. (1993) Molecular cloning and characterization of a sym plasmid locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257. Mol Microbiol 9: 17-29.
48. Menard, R., Sansonetti, P.J., and Parsot, C. (1993) Non-polar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
49. Mindrinos, M., Katagiri, F., Yu, G.L., and Ausubel, P.M. (1994) The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.
50. Minsavage, G.V., Dahlbeck, D., Whalen, M.C., Kearney, B., Bonas, U., Staskawicz, B.J., et al. (1990) Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv. vesicatona-peppei interactions. Mol Plant-Microbe Interact 3: 41-47.
51. -) mutant of Erwinia carotovora subspecies atroseptica is defective in flagella assembly proteins that are conserved in plant and animal bacterial pathogens. Mol Microbiol 9: 343-356.
52. Murillo, J., Shen, H., Gerhold, D., Sharma, A., Cooksey, D.A., and Keen, N.T. (1994) Characterization of pPT23B, the plasmid involved in syringolide production by Pseudomonas syringae pv. tomato PT23. Plasmid 31: 275-287.
53. Ohnishi, K., Fan, F., Schoenhals, G.J., Kihara, M., and Macnab, R.M. (1997) The FliO, FliP, and FliR proteins of Salmonella typhimurium: putative components for flagellar assembly. J Bacteriol 179: 6092-6099.
54. Prentki, P., and Krisch, H.M. (1984) In vitro insertion mutagenesis with a selectable DNA fragment. Gene 29: 303-313.
55. Ramakrishnan, G., Zhao, J.L., and Newton, A. (1994) Multiple structural proteins are required for both transcriptional activation and negative autoregulation of Caulobacter crescentus flagellar genes. J Bacteriol 176: 7587-7600.
56. Richardson, W.D., Roberts, B.L., and Smith, A.E. (1986) Nuclear location signals in polyoma virus large-T. Cell 44: 77-85.
57. Rihs, H.P., Jans, D.A., Fan, H., and Peters, R. (1991) The rate of nuclear cytoplasmic protein transport is determined by the casein kinase II site flanking the nuclear localization sequence of the SV40 T-antigen. EMBO J 10: 633-639.
58. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E.L., Kalkkinen, N., Romantschuk, M., et al. (1997) Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 94: 3459-3464.
59. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
60. Sasakawa, C., Komatsu, K., Tobe, T., Suzuki, T., and Yoshikawa, M. (1993) Eight genes in region 5 that form an operon are essential for invasion of epithelial cells by Shigella flexneri 2a. J Bacteriol 175: 2334-2346.
61. Schulte, R., and Bonas, U. (1992a) Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hypersensitivity on pepper and tomato, is plant inducible. J Bacteriol 174: 815-823.
62. Schulte, R., and Bonas, U. (1992b) A Xanthomonas pathogenicity locus is induced by sucrose and sulfur-containing amino acids. Plant Cell 4: 79-86.
63. Staskawicz, B.J., Dahlbeck, D., Keen, N., and Napoli, C. (1987) Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J Bacteriol 169: 5789-5794.
64. Van den Ackerveken, G., Marois, E., and Bonas, U. (1996) Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 1307-1316.
65. Van Gijsegem, F., Gough, C., Zischek, C., Niqueux, E., Arlat, M., Genin, S., et al. (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. Varagona, M.J., Schmidt, R.J., and Raikhel, N.V. (1992) Nuclear localization signal(s) required for nuclear targeting of the maize regulatory protein Opaque-2. Plant Cell 4: 1213-1227.
67. Venkatesan, M.M., Buysse, J.M., and Oaks, E.V. (1992) Surface presentation of Shigella flexneri invasion plasmid antigens requires the products of the spa locus. J Bacteriol 174: 1990-2001.
68. Vieira, J., and Messing, J. (1987) Production of single-stranded plasmid DNA. Methods Enzymol 153: 3-11.
69. Wei, Z.M., Laby, R.J.. Zumoff, C.H., Bauer, D.W., He, S.Y., Collmer, A., et al. (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257: 85-88.
70. Wengelnik, K., and Bonas, U. (1996) HrpXv, an AraC-type regulator, activates expression of five out of six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol 178: 3462-3469.
71. Wengelnik, K., Marie, C., Russel, M., and Bonas, U. (1996a) Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J Bacteriol 178: 1061-1069.
72. Wengelnik, K., Van den Ackerveken, G., and Bonas, U. (1996b) HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol Plant-Microbe Interact 9: 704-712.
73. Whalen, M.C., Wang, J.F., Carland, F.M., Heiskell, M.E., Dahlbeck, D., Minsavage, G.V., et al. (1993) Avirulence gene avRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol Plant-Microbe Interact 6: 616-627.
74. Zhuang, W.Y., and Shapiro, L. (1995) Caulobacter FliQ and FliR membrane proteins, required for flagellar biogenesis and cell division, belong to a family of virulence factor export proteins. J Bacteriol 177: 343-356.