Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum

Journal of Bacteriology

Volumn 188, Issue 10, 2006, Pages 3697-3708

  Yao, Jian ^a   Allen, Caitilyn ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; CARBOXYLIC ACID; DNA; PROTEIN;

ADAPTATION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CHEMOTAXIS; CONTROLLED STUDY; DNA SEQUENCE; FITNESS; GENETIC TRAIT; MUTANT; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RALSTONIA SOLANACEARUM; SOUTHERN BLOTTING; TOMATO;

CHEMOTAXIS; ESCHERICHIA COLI; GENE DELETION; KINETICS; LYCOPERSICON ESCULENTUM; MOVEMENT; MUTAGENESIS, SITE-DIRECTED; MUTATION; PLANT DISEASES; PLASMIDS; RALSTONIA SOLANACEARUM; VIRULENCE;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; RALSTONIA SOLANACEARUM;

EID: 33646595316     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.10.3697-3708.2006     Document Type: Article

References (57)

1. Adler, J. 1966. Chemotaxis in bacteria. Science 153:708-716.
2. Alexandre, G., S. Greer-Phillips, and I. B. Zhulin. 2004. Ecological role of energy taxis in microorganisms. FEMS Microbiol. Rev. 28:113-126.
3. Allen, C., Y. Huang, and L. Sequeira. 1991. Cloning of genes affecting polygalacturonase production in Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4:147-154.
4. Andermann, T. M., Y.-T. Chen, and K. M. Ottemann. 2002. Two predicted chemoreceptors of Helicobacter pylori promote stomach infection. Infect. Immun. 70:5877-5881.
5. Arlat, M., C. L. Gough, C. Zischek, P. A. Barberis, A. Trigalet, and C. A. Boucher. 1992. Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum. Mol. Microbiol. 6:3065-3076.
6. 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, N.Y.
7. Blair, D. F. 1995. How bacteria sense and swim. Annu. Rev. Microbiol. 49:489-520.
8. Borkovich, K. A., and M. I. Simon. 1990. The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63:1339-1348.
9. 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.
10. Brencic, A., and S. C. Winans. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:155-194.
11. Caetano-Anollés, G., D. K. Crist-Estes, and W. D. Bauer. 1988. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J. Bacteriol. 170:3164-3169.
12. Conley, M. P., A. J. Wofle, D. F. Blair, and H. C. Berg. 1989. Both CheA and CheW are required for reconstitution of chemotactic signaling in Escherichia coli. J. Bacteriol. 171:5190-5193.
13. Cook, D., E. Barlow, and L. Sequeira. 1989. Genetic diversity of Pseudomonas solanacearum: detection of restriction fragment length polymorphisms with DNA probes that specify virulence and the hypersensitive response. Mol. Plant-Microbe Interact. 2:113-121.
14. Cuppels, D. A. 1988. Chemotaxis by Pseudomonas syringae pathovar tomato. Appl. Environ. Microbiol. 54:629-632.
15. 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.
16. de Weert, S., H. Vermeiren, I. Mulders, I. Kuiper, N. Hendrickx, G. Bloemberg, J. Vanderleyden, R. De Mot, and B. J. Lugtenberg. 2002. Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol. Plant-Microbe Interact. 15:1173-1180.
17. Dharmatilake, A. J., and W. D. Bauer. 1992. Chemotaxis of Rhizobium meliloti toward nodulation gene-inducing compounds from alfalfa roots. Appl. Environ. Microbiol. 58:1153-1158.
18. Fegan, M., and P. Prior. 2005. How complex is the "Ralstonia solanacearum" species complex?, p. 449-461. In C. Allen, P. Prior, and A. C. Hayward (ed.), Bacterial wilt disease and the Ralstonia solanacearum species complex. APS Press, St. Paul, Minn.
19. 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. Gonzalez, 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.
20. Gaworzewska, E. T., and M. J. Carlile. 1982. Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants. J. Gen. Microbiol. 128:1179-1188.
21. Greer-Phillips, S. E., B. B. Stephens, and G. Alexandre. 2004. An energy taxis transducer promotes root colonization by Azospirillum brasilense. J. Bacteriol. 186:6595-6604.
22. Harwood, C. S., M. Rivelli, and L. N. Ornston. 1984. Aromatic acids are chemoattractant for Pseudomonas putida. J. Bacteriol. 160:622-628.
23. Hayward, A. C. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87.
24. Hendrick, C., and L. Sequeira. 1984. Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl. Environ. Microbiol. 48:94-101.
25. 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.
26. Jeziore-Sassoon, Y., P. A. Hamblin, C. A. Bootle-Wilbraham, P. S. Poole, and J. P. Armitage. 1998. Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides. Microbiology 144:229-239.
27. Kelman, A. 1954. The relationship of pathogenicity of Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44:693-695.
28. Liu, H., Y. Kang, S. Genin, M. A. Schell, and T. P. Denny. 2001. Twitching motility of Ralstonia solanacearum requires a type IV pilus system. Microbiology 147:3215-3229.
29. 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.
30. 1 towards sugars involves a highly sensitive chemotaxis system. J. Gen. Microbiol. 134:1427-1432.
31. Lugtenberg, B. J., L. V. Kravchenko, and M. Simons. 1999. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas bicontrol strains and role in rhizosphere colonization. Environ. Microbiol. 1:439-446.
32. Macnab, R. M. 1996. Flagella and motility, p. 123-145. In F. C. Neidhardt, R. I. 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: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
33. McGarvey, J. A., T. P. Denny, and M. A. Schell. 1999. Spatial-temporal and quantitative analysis of growth and EPSI production by Ralstonia solanacearum in resistant and susceptible tomato cultivars. Phytopathology 89:1233-1239.
34. Menard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
35. Meng, Y., Y. Li, C. D. Galvani, G. Hao, J. N. Turner, T. J. Burr, and H. C. Hoch. 2005. Upstream migration of Xyleila fastidiosa via pilus-driven twitching motility. J. Bacteriol. 187:5560-5567.
36. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
37. Okon, Y., L. Cakmakci, I. Nur, and I. Chet. 1980. Aerotaxis and chemotaxis in Azospririllum brasilense: a note. Microb. Ecol. 6:277-280.
38. O'Toole, R., D. L. Milton, and H. Wolf-Watz. 1996. Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum. Mol. Microbiol. 19:625-637.
39. Parkinson, J. S. 1976. cheA, cheB, and cheC genes of Escherichia coli and their role in chemotaxis. J. Bacteriol. 126:758-770.
40. Pfund, C., J. K. Tans-Kersten, M. Dunning, C. Allen, and A. F. Bent. 2004. Flagellin is not a major defense elicitor in Ralstonia solanacearum cells or extracts applied to Arabidopsis thaliana. Mol. Plant-Microbe Interact. 17:696-706.
41. Raymundo, A. K., and S. M. Ries. 1980 Chemotaxis of Erwinia amylovora. Phytopathology 70:1066-1069.
42. Salanoubat, M., S. Genin, F. Artiguenave, J. Gouzy, S. Mangenot, M. Arlat, A. Billault, P. Brottier, J.-C. 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.
43. Schell, M., D. P. Roberts, and T. P. Denny. 1988. Analysis of the Pseudomonas solanacearum polygalacturonase encoded by pglA and its involvement in phytopathogenicity. J. Bacteriol. 170:4501-4508.
44. Schmitt, R. 2002. Sinorhizobial chemotaxis: a departure from the enterobacterial paradigm. Microbiology 148:627-631.
45. Schweizer, H. P. 1993. Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831-833.
46. Simons, M., H. P. Permentier, L. A. de Weger, C. A. Wijffelman, and B. J. Lugtenberg. 1997. Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol. Plant-Microbe Interact. 10:102-106.
47. Staskawicz, B., D. Dahlbeck, N. Keen, and C. Napoli. 1986. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
48. Stock, J. B., and M. G. Surette. 1996. Chemotaxis, p. 1103-1129. In F. C. Neidhardt, R. I. 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: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
49. Swanson, J. K., J. Yao, J. K. Tans-Kersten, and C. Allen. 2005. Behavior of Ralstonia solanacearum race 3 biovar 2 during latent and active infection of geranium. Phytopathology 95:136-143.
50. 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.
51. Tans-Kersten, J., H. Huang, and C. Allen. 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183:3597-3605.
52. Tans-Kersten, J. K., D. Brown, and C. Allen. 2004. Swimming motility, a virulence factor of Ralstonia solanacearum, is regulated by FlhDC and by the plant host environment. Mol. Plant-Microbe Interact. 17:686-695.
53. Terry, K., S. M. Williams, L. Connolly, and K. M. Ottemann. 2005. Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect. Immun. 73:803-811.
54. Vande Broek, A., and J. Vanderleyden. 1995. The role of bacterial motility, chemotaxis, and attachment in bacteria-plant interactions. Mol. Plant-Microbe Interact. 8:800-810.
55. Vasse, J., P. Frey, and A. Trigalet. 1995. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 8:241-251.
56. Yu, H. S., and M. Alam. 1997. An agarose-in-plug bridge method to study chemotaxis in the archaeon Halobacterium salinarum. FEMS Microbiol. Lett. 156:265-269.
57. Zhulin, I. B., and B. L. Taylor. 1995. Chemotaxis in plant-associated bacteria: the search for the ecological niche, p. 451-459. In I. Fendrik, M. Del Gallo, J. Vanderleyden, and M. de Zamaroczy (ed.), Azospririllum VI and related microorganisms: genetics, physiology, and ecology, vol. G37. Springer-Verlag, Berlin, Germany.