Using the Ralstonia solanacearum tat secretome to identify bacterial wilt virulence factors

Applied and Environmental Microbiology

Volumn 73, Issue 12, 2007, Pages 3779-3786

  González, Enid T ^a,b   Brown, Darby G ^a,c   Swanson, Jill K ^a   Allen, Caitilyn ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

PHENOTYPE; PHYTOPATHOGEN; POLYGALACTURONASE; RALSTONIA SOLANACEARUM; TRANSLOCATION;

AMINO ACIDS; BACTERIA; ENZYME KINETICS; GENE EXPRESSION; MUTAGENESIS; PLANTS (BOTANY); PROTEINS;

PATHOGENS;

BINDING PROTEIN; GENE PRODUCT; TWIN ARGININE TRANSLOCATION SECRETION SYSTEM; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIUM; BIOASSAY; GENE EXPRESSION; GENETIC ANALYSIS; IDENTIFICATION METHOD; MUTATION; PHENOTYPE; VIRULENCE;

ACID TOLERANCE; ARTICLE; ASSAY; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL WILT; BACTERIUM CULTURE; BIOINFORMATICS; CULTURE MEDIUM; GENE FUNCTION; GENE MUTATION; MOLECULAR CLONING; NATURALISTIC SOIL SOAK ASSAY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLEIOTROPY; PREDICTION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; RALSTONIA SOLANACEARUM; RSC1651 GENE; RSP1521 GENE; RSP1575 GENE; TATC GENE; TOMATO; UPREGULATION;

BACTERIAL PROTEINS; BASE SEQUENCE; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA PRIMERS; GENETIC COMPLEMENTATION TEST; LYCOPERSICON ESCULENTUM; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PLANT DISEASES; RALSTONIA SOLANACEARUM; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; RALSTONIA SOLANACEARUM;

EID: 34250795104     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02999-06     Document Type: Article

References (44)

1. Allen, C., Y. Huang, and L. Sequeira. 1991. Cloning of genes affecting polygalacturonase production in Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4:147-154.
2. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. Seidman, J. Smith, and K. Struhl. 1995. Short protocols in molecular biology, 3rd ed. John Wiley and Sons, New York, NY.
3. Berks, B. C., T. Palmer, and F. Sargent. 2003. The TAT protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47:187-254.
4. Boucher, C., P. Barberis, A. Trigalet, and D. Demery. 1985. Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J. Gen. Microbiol. 131:2449-2457.
5. Bronstein, P. A., M. Marrichi, S. Cartinhour, D. J. Schneider, and M. P. DeLisa. 2005. Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J. Bacteriol. 187:8450-8461.
6. Brown, D. G., and C. Allen. 2004. Ralstonia solanacearum genes induced during growth in tomato: an inside view of bacterial wilt. Mol. Microbiol. 53:1641-1660.
7. Caldelari, I., S. Mann, C. Crooks, and T. Palmer. 2006. The Tat pathway of the plant pathogen Pseudomonas syringae is required for virulence. Mol. Plant-Microbe Interact. 19:200-212.
8. Christie, P., K. Atmakuri, V. Krishnamoorthy, S. Jakubowski, and E. Cascales. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
9. Cornelis, G. R., and F. VanGijsegem. 2000. Assembly and function of type III secretion systems. Annu. Rev. Microbiol. 54:735-774.
10. Cristobal, S., J.-W. de Gier, H. Nielsen, and G. von Heijne. 1999. Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J. 18:2982-2990.
11. Denny, T. P., and S. R. Baek. 1991. Genetic evidence that extracellular polysaccharide is a virulence factor of Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4:198-206.
12. Dilks, K., R. W. Rose, E. Hartmann, and M. Pohlschroder. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185:1478-1483.
13. Ding, Z., and P. J. Christie. 2003. Agrobacterium lumefaciens twin-arginine-dependent translocation is important for virulence, flagellation, and chemotaxis but not type IV secretion. J. Bacteriol. 185:760-771.
14. Gabriel, D. W., C. Allen, M. Schell, T. P. Denny, J. T. Greenberg, Y. P. Duan, Z. Flores-Cruz, Q. Huang, J. M. Clifford, G. Presting, E. T. González, J. Reddy, J. Elphinstone, J. Swanson, J. Yao, V. Mulholland, L. Liu, W. Farmerie, M. Patnaikuni, B. Balogh, D. Norman, A. Alvarez, J. A. Castillo, J. Jones, G. Saddler, T. Walunas, A. Zhukov, and N. Mikhailova. 2006. Identification of open reading frames unique to a select agent: Ralstonia solanacearum race 3 biovar 2. Mol. Plant-Microbe Interact. 19:69-79.
15. Gonzalez, E. T., and C. Allen. 2003. Characterization of a Ralstonia solanacearum operon required for polygalacturonate degradation and uptake of galacturonic acid. Mol. Plant-Microbe Interact. 16:536-544.
16. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
17. Harding, S. A., O. Suk-Heung, and D. M. Roberts. 1997. Transgenic tobacco expressing a foreign calmodulin gene shows an enhanced production of active oxygen species. EMBO J. 16:1137-1144.
18. Hayward, A. C. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87.
19. Heikkila, M. P., U. Honsisch, P. Wunsch, and W. G. Zumft. 2001. Role of the Tat transport system in nitrous oxide reductase translocation and cytochrome cd1 biosynthesis in Pseudomonas stutzeri. J. Bacteriol. 183:1663-1671.
20. Hendrick, C., and L. Sequeira. 1984. Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl. Environ. Microbiol. 48:94-101.
21. Huang, Q., and C. Allen. 1997. An exo-poly-α-D- galacturonosidase, PehB, is required for wild-type virulence of Ralstonia solanacearum. J. Bacteriol. 179:7369-7378.
22. Huang, Q., and C. Allen. 2000. Polygalacturonases are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants. Physiol. Mol. Plant Pathol. 57:77-83.
23. Hugouvieux-Cotte-Pattat, N., G. Condemine, W. Nasser, and S. Reverchon. 1996. Regulation of pectinolysis in Erwinia chrysanthemi. Annu. Rev. Microbiol. 50:213-257.
24. Kang, Y., J. Huang, G. Mao, L. He, and M. A. Schell. 1994. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol. Plant-Microbe Interact. 7:370-377.
25. Kelman, A. 1954. The relationship of pathogenicity of Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44:693-695.
26. Liu, H., S. Zhang, M. A. Schell, and T. P. Denny. 2005. Pyramiding unmarked deletions in Ralstonia solanacearum shows that secreted proteins in addition to plant cell-wall-degrading enzymes contribute to virulence. Mol. Plant-Microbe Interact. 18:1296-1305.
27. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Press, Cold Spring Harbor, NY.
28. Ochsner, U. A., A. Snyder, A. I. Vasil, and M. L. Vasil. 2002. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc. Natl. Acad. Sci. USA 99:8312-8317.
29. Pradel, N., C. Ye, V. Livrelli, J. Xu, B. Joly, and L.-F. Wu. 2003. Contribution of the twin arginine translocation system to the virulence of enterohemorrhagic Escherichia coli O157:H7. Infect. Immun. 71:4908-4916.
30. Reference deleted.
31. Preston, G., D. J. Studholme, and I. Calelari. 2005. Profiling the secretomes of plant pathogenic proteobacteria. FEMS Microbiol. Rev. 29:331-360.
32. Pugsley, A. P., O. Francetic, A. J. Driessen, and V. deLorenzo. 2004. Getting out: protein traffic in prokaryotes. Mol. Microbiol. 52:3-11.
33. Roberts, D. P., T. P. Denny, and M. Schell. 1988. Cloning of the egl gene of Pseudomonas solanacearum and analysis of its role in phytopathogenicity. J. Bacteriol. 170:1445-1451.
34. Salanoubat, M., S. Genin, F. Artiguenave, J. Gouzy, S. Mangenot, M. Arlat, A. Billault, P. Brottier, J. Camus, L. Cattolico, M. Chandler, N. Choisne, C. Claudel-Renard, S. Cunnac, N. Demange, C. Gaspin, M. Lavie, A. Moisan, C. Robert, W. Saurin, T. Schiex, P. Siguier, P. Thebault, M. Whalen, P Wincker, M. Levy, J. Weissenbach, and C. A. Boucher. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502.
35. Schell, M. A. 2000. Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory array. Annu. Rev. Phytopathol. 38: 263-292.
36. Schweizer, H. P. 1993. Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831-833.
37. Stanley, N. R., T. Palmer, and B. C. Berks. 2000. The twin-arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli. J. Biol. Chem. 275:11591-11596.
38. Staskawicz, B., D. Dahlbeck, N. Keen, and C. Napoli. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
39. Tans-Kersten, J., Y. Guan, and C. Allen. 1998. Ralstonia solanacearum pectin methylesterase is required for growth on methylated pectin but not for bacterial wilt virulence. Appl. Environ. Microbiol. 64:4918-4923.
40. Tans-Kersten, J., H. Huang, and C. Allen. 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183:3597-3605.
41. Vinuesa, P., F. Newumann-Silkow, C. Pacios-Bras, H. P. Spaink, E. Martinez-Romero, and D. Werner. 2003. Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol. Plant-Microbe Interact. 16:159-168.
42. Voulhoux, R., G. Ball, B. Ize, M. L. Vasil, A. Lazdunski, L.-F. Wu, and A. Filloux. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 20:6735-6741.
43. Wirawan, I. G. P., H. W. Kang, and M. Kojima. 1993. Isolation and characterization of a new chromosomal virulence gene of Agrobacterium tumefaciens. J. Bacteriol. 175:3208-3212.
44. Yao, J., and C. Allen. 2006. Chemotaxis is required for virulence and competitive fitness in the bacterial wilt pathogen Ralstonia solanacearum. J. Bacteriol. 188: 3697-3708.