Genetic screening of Hrp type III-related pathogenicity genes controlled by the HrpB transcriptional activator in Ralstonia solanacearum

Molecular Microbiology

Volumn 54, Issue 4, 2004, Pages 863-875

  Mukaihara, Takafumi ^a   Tamura, Naoyuki ^a   Murata, Yukio ^a   Iwabuchi, Masaki ^a  

^a Research Institute for Biological Science OKAYAMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA GALACTOSIDASE; CYTARABINE; GENTAMICIN; HYDROLASE; KANAMYCIN; LACTOYLGLUTATHIONE LYASE; LEUCINE; NALIDIXIC ACID; NUDIX HYDROLASE; SPECTINOMYCIN; SPERMIDINE SYNTHASE; STREPTOMYCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HRPB; TRANSPOSASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIUM PILUS; CELL SURFACE; CONTROLLED STUDY; DNA SEQUENCE; ELECTROPORATION; ESCHERICHIA COLI; GENE EXPRESSION; GENE ISOLATION; GENETIC SCREENING; HPAB GENE; HPAZ GENE; HRP GENE; HRPY GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; NULL ALLELE; OPEN READING FRAME; PATHOGENICITY; PHENOTYPE; PLANT DISEASE; PRIORITY JOURNAL; PROMOTER REGION; RALSTONIA SOLANACEARUM; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION; TRANSPOSON;

BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTATION; OPEN READING FRAMES; PHENOTYPE; RALSTONIA SOLANACEARUM; TOBACCO; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; RALSTONIA; RALSTONIA SOLANACEARUM; TRANSPOSONS;

EID: 8544253953     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04328.x     Document Type: Article

References (53)

1. Aizawa, S.-I. (2001) Bacterial flagella and type III secretion systems. FEMS Microbiol Lett 202: 157-164.
2. Alexeyev, M.F., Shokolenko, I.N., and Croughan, T.P. (1995) New mini-Tn5 derivatives for insertion mutagenesis and genetic engineering in Gram-negative bacteria. Can J Microbiol 41: 1053-1055.
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 Bacterial 179: 5655-5662.
4. Arlat, M., Gough, C.L., Zischek, C., Barberis, A., Trigalet, A., and Boucher, C.A. (1992) Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum. Mol Plant Microbe Interact 5: 187-193.
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. Boch, J., Joardar, V., Gao, L., Robertson, T.L., Lim, M., and Kunkel, B.N. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44: 73-88.
7. Boucher, C.A., Barberis, P.A., Trigalet, A.P., and Demery, D. (1985) Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J Gen Microbiol 131: 2449-2457.
8. Boucher, C.A., Van Gijsegem, F., Barberies, P.A., Arlat, M., and Zischek, C. (1987) Pseudomanas solanacearum genes controlling both pathogenicity on tomato and hypersensitivity on tobacco are clustered. J Bacteriol 169: 5626-5633.
9. Büttner, D., and Bonas, U. (2002) Getting across - bacterial type III effector proteins on their way to the plant cell. EMBO J 21: 5313-5322.
10. Casper-Lindley, C., Dahlbeck, D., Clark, E.T., and Staskawicz, B.J. (2002) Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc Natl Acad Sci USA 99: 8336-8341.
11. Cornelis, G.R., and Van Gijsegem, F. (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54: 735-774.
12. Cunnac, S., Boucher, C., and Genin, S. (2004) Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the type III secretion system and effector genes in Ralstonia solanacearum. J Bacteriol 186: 2309-2318.
13. 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.
14. Fouts, D.E., Abramovitch, R.B., Alfano, J.R., Baldo, A.M., Buell, C. R., Cartinhour, S., et al. (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.
15. Galán, J.E., and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
16. Genin, S., and Boucher, C. (2002) Ralstonia solanacearum: secrets of a major pathogen unveiled by analysis of its genome. Mol Plant Pathol 3: 111-118.
17. Genin, S., Gough, C.L., Zischek, C., and Boucher, C.A. (1992) Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol Microbiol 6: 3065-3076.
18. Gophna, U., Ron, E.Z., and Graur, D. (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312: 151-163.
19. Guéneron, M., Timmers, A.C.J., Boucher, C.A., and Arlat, M. (2000) Two novel proteins, PopB, which has functional nuclear localization signals, and PopC, which has a large leucine-rich repeat domain, are secreted through the Hrp-secretion apparatus of Ralstonia solanacearum. Mol Microbiol 36: 261-277.
20. Guttman, D.S., Vinatzer, B.A., Sarkar, S.F., Ranall, M.V., Kettler, G., and Greenberg, J.T. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726.
21. Hartman, A.B., Venkatesan, M., Oaks, E.V., and Buysse, J.M. (1990) Sequence and molecular characterization of a multicopy invasion plasmid antigen gene, ipaH, of Shigella flexneri. J Bacteriol 172: 1905-1915.
22. Hayward, A.C. (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 29: 65-87.
23. Hueck, C.J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
24. Jain, C. (1993) New improved lacZ gene fusion vectors. Gene 133: 99-102.
25. Jin, Q., and He, S.Y. (2001) Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294: 2556-2558.
26. Kang, Y., Liu, H., Genin, S., Schell, M.A., and Denny, T.P. (2002) Ralstonia solanacearum requires type 4 pili to adhere to multiple surfaces and for natural transformation and virulence. Mol Microbiol 46: 427-437.
27. Keen, N.T., Tamaki, D., Kobayashi, D., and Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70: 191-197.
28. Kim, J.-G., Park, B.K., Yoo, C.-H., Jeon, E., Oh, J., and Hwang, I. (2003) Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J Bacteriol 185: 3155-3166.
29. Kobe, B., and Deisenhofer, J. (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19: 415-421.
30. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., et al. (1998) Supermolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605.
31. Lavie, M., Shillington, E., Eguiluz, C., Grimsley, N., and Boucher, C. (2002) PopP1, a new member of the YopJ/AvrRxv family of type III effector proteins, acts as a host specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol Plant Microbe Interact 15: 1058-1068.
32. Leach, J.E., and White, F.F. (1996) Bacterial avirulence genes. Annu Rev Phytopathol 34: 153-179.
33. Miller, J.H. (1992) A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Nakano, Y., Yoshida, Y., Yamashita, Y., and Koga, T. (1995) Construction of a series of pACYC-derived plasmid vectors. Gene 162: 157-158.
35. Noël, L., Thieme, F., Nennstiel, D., and Bonas, U. (2001) cDNA-AFLP analysis unravels a genome-wide n/pG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol Microbiol 41: 1271-1281.
36. - bacteria. Gene 133: 23-30.
37. Petnicki-Ocwieja, T., Schneider, D.J., Tam, V.C., Chancey, S.T., Shan, L.T., Jamir, T., et al. (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.
38. Roine, E., Wei, W.S., Yuan, J., Nurmiaho-Lassila, E.L., Kalkkinen, N., Romantschuk, M., and He, S.Y. (1997) Hrp pilus: a hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 94: 3459-3464.
39. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., et al. (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415: 497-502.
40. Scholz, P., Haring, V., Wittmann-Liebold, B., Ashman, K., Bagdssarian, M., and Scherzinger, E. (1989) Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 75: 271-288.
41. da Silva, A.C., Ferro, J.A., Reinach, F.C., Farah, C.S., Furlan, L.R., Quaggio, R.B., et al. (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: 459-463.
42. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biol Technology 1: 784-791.
43. Simons, R.W., Houman, F., and Kleckner, N. (1987) Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96.
44. Sory, M.P., and Cornelis, G.R. (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
45. Staskawicz, B.J., Mudget, M.B., Dangle, J.L., and Galán, J.E. (2001) Common and contrasting themes of plant and animal diseases. Science 292: 2285-2289.
46. Tamano, K., Aizawa, S., Katayama, E., Nonaka, T., Imajoh-Ohmi, S., Kuwae, A., et al. (2000) Supermolecular structure of the Shigella type III secretion machinery: the needle part is changeable in length and essential for delivery of effectors. EMBO J 19: 3876-3887.
47. Tans-Kersten, J., Huang, H., and Allen, C. (2001) Ralstonia solanacearum needs motility for invasive virulence on tomato. J Bacteriol 183: 3597-3605.
48. Van Gijsegem, F., Zischek, C., Gough, C., Niqueux, E., Arlat, M., Genin, S., et al. (1995) The hrp locus of Pseudomonas solanacearum that 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.
49. Van Gijsegem, F., Vasse, J., Camus, J.C., Marenda, M., and Boucher, C. (2000) Ralstonia solanacearum produces Hrp-dependent pili that are required for PopA secretion but not for attachment of bacteria to plant cells. Mol Microbiol 36: 249-260.
50. 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 III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc Natl Acad Sci USA 97: 2247-2252.
51. Wengelnik, K., and Bonas, U. (1996) HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol 178: 3462-3469.
52. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.
53. Zwiesler-Vollick, J., Plovanich-Jones, A., Nomura, K., Bandyopadhyay, S., Joardar, V., Kunkel, B.N., and He, S.Y. (2002) Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol 45: 1207-1218.