Ralstonia solanacearum needs Flp pili for virulence on potato

Molecular Plant-Microbe Interactions

Volumn 25, Issue 4, 2012, Pages 546-556

  Wairuri, Charles K ^a   Van Der Waals, Jacquie E ^a   Van Schalkwyk, Antoinette ^b   Theron, Jacques ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b Inqaba Biotechnical Industries   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; FIMBRIA PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BIOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; POTATO; RALSTONIA SOLANACEARUM; TIME; VIRULENCE;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; DNA, BACTERIAL; FIMBRIAE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; PLANT DISEASES; RALSTONIA SOLANACEARUM; SOLANUM TUBEROSUM; TIME FACTORS; VIRULENCE;

BACTERIA (MICROORGANISMS); IVA; RALSTONIA SOLANACEARUM; SOLANUM TUBEROSUM;

EID: 84858979497     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-11-0166     Document Type: Article

References (75)

1. Aldon, D., Brito, B., Boucher, C, and Genin, S. 2000. A bacterial sensor of plant-cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO (Eur. Mol. Biol. Organ.) J. 19:2304-2314. (Pubitemid 30259011)
2. Allen, C. A., Huang, Y., and Sequeira, L. 1991. Cloning of genes affecting polygalacturonase production in Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4:147-154.
3. Araud-Razou, I., Vasse, J., Montrozier, H., Etchebar, C, and Trigalet, A. 1998. Detection and visualization of the major acidic exopolysaccha-ride of Ralstonia solanacearum and its role in tomato root infection and vascular colonization. Eur. J. Plant Pathol. 104:795-809. (Pubitemid 29072947)
4. Bahar, O., Goffer, T., and Burdman, S. 2009. Type IV pili are required for virulence, twitching motility, and biofilm formation of Acidovorax avenae subsp. citrulli. Mol. Plant-Microbe Interact. 22:909-920.
5. Bernard, C. S., Bordi, C., Termine, E., Filloux, A., and de Bentzmann, S. 2009. Organization and PprB-dependent control of the Pseudomonas aeruginosa tad locus, involved in Flp pilus biology. J. Bacteriol. 191:1961-1973.
6. Bhattacharjee, M. K., Kachlany, S. C., Fine, D. H., and Figurski, D. H. 2001. Nonspecific adherence and fibril biogenesis by Actinobacillus actinomycetemcomitans: TadA protein is an ATPase. J. Bacteriol. 183:5927-5936. (Pubitemid 32917412)
7. Brito, B., Marenda, M., Barberis, P., Boucher, C., and Genin, S. 1999. prhJ and hrpG, two new components of the plant signal dependent regulatory cascade controlled by PrhA in Ralstonia solanacearum. Mol. Microbiol. 31:237-251. (Pubitemid 29012163)
8. Brumbley, S. M., and Denny, T. P. 1990. Cloning of phcA from wild-type Pseudomonas solanacearum, a gene that when mutated alters expression of multiple traits that contribute to virulence. J. Bacteriol. 172:5677-5685. (Pubitemid 20317103)
9. Buttner, D., and Bonas, U. 2002. Getting across-bacterial type III effector proteins on their way to the plant cell. EMBO (Eur. Mol. Biol. Organ.) J. 21:5313-5322. (Pubitemid 35231011)
10. Chamot-Rooke, J., Mikaty, G., Malosse, C, Soyer, M., Dumont, A., Gault, J., Imhaus, A. F, Martin, P., Trellet, M., Clary, G., Chafey, P., Camoin, L., Nilges, M., Nassif, X., and Duménil, G. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331:778-782.
11. Clock, S. A., Planet, P. J., Perez, B. A., and Figurski, D. H. 2008. Outer membrane components of the Tad (tight adherence) secretion of Aggre-gatibacter actinomycetemcomitans J. Bacteriol. 190:980-990. (Pubitemid 351170942)
12. Cohen, S. N., Chang, A. C. Y., and Hsu, L. 1972. Nonchromosomal antibiotic resistance in bacteria: Genetic transformation of Escherichia coli by R-factor DNA. Proc. Natl. Acad. Sci. U.S.A. 69:2110-2114.
13. Craig, L., and Li, J. 2008. Type IV pili: Paradoxes in form and function. Curr. Opin. Struct. Biol. 18:267-277.
14. Cunnac, S., Occhialini, A., Barberis, P., Boucher, C, and Genin, S. 2004. Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: Identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol. Microbiol. 53:115-128. (Pubitemid 38901384)
15. Danhorn, T, and Fuqua, C. 2007. Biofilm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61:401-422. (Pubitemid 350058215)
16. de Bentzmann, S., Aurouze, M., Ball, G., and Filloux, A. 2006. FppA, a novel Pseudomonas aeruginosa prepilin peptidase involved in assembly of type IVb pili. J. Bacteriol. 188:4851-4860. (Pubitemid 43956083)
17. Denny, T. P., and Baek, S. R. 1991. Genetic evidence that extracellular polysaccharide is a virulence factor of Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 4:198-206.
18. Denny, T. P., Makini, F W., and Brumbley, S. M. 1988. Characterization of Pseudomonas solanacearum Tn5 mutants deficient in extracellular polysaccharide. Mol. Plant-Microbe Interact. 1:215-223.
19. Fernandez, L., Marquez, I., and Guijarro, J. A. 2004. Identification of specific in vivo-induced genes in Yersinia ruckeri and analysis of rucker-bactin, a catecholate siderophore iron acquisition system. Appl. Environ. Microbiol. 70:5199-5207. (Pubitemid 39279590)
20. Fock, I., Collonnier, C, Purwito, A., Luisetti, J., Souvannavong, V, Vedel, F., Servaes, A., Ambroise, A., Kodja, H., Ducreux, G., and Sihachakr, D. 2000. Resistance to bacterial wilt in somatic hybrids between Solanum tuberosum and Solanum phureja. Plant Sci. 160:165-176. (Pubitemid 32065979)
21. Fock, I., Collonnier, C, Luisetti, J., Purwito, A., Souvannavong, V, Vedel, F., Servaes, A., Ambroise, A., Kodja, H., Ducreux, G., and Sihachakr, D. 2001. Use of Solanum stenotomum for introduction of resistance to bacterial wilt in somatic hybrids of potato. Plant Physiol. Biochem. 39:899-908. (Pubitemid 32974247)
22. Frey, P., Prior, P., Marie, C, Koutoujansky, A., Trigalet-Demery, D., and Trigalet, A. 1994. Hrp-mutants of Pseudomonas solanacearum as potential biocontrol agents of tomato bacterial wilt. Appl. Environ. Microbiol. 60:3175-3181.
23. Fronzes, R., Remaut, H., and Waksman, G. 2008. Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO (Eur. Mol. Biol. Organ.) J. 27:2271-2280.
24. Fuller, T. E., Kennedy, M. J., and Lowery, D. E. 2000. Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature tagged mutagenesis. Microb. Pathog. 29:25-38.
25. Genin, S., and Boucher, C. A. 2004. Lessons learned from the genome analysis of Ralstonia solanacearum. Annu. Rev. Phytopathol. 42:107-134. (Pubitemid 39308508)
26. Gerlach, R. G., and Hensel, M. 2007. Protein secretion systems and adhesins: The molecular armory of gram-negative pathogens. Int. J. Med. Microbiol. 297:401-415. (Pubitemid 47375177)
27. Gonzalez, E. T, and Allen, C. 2003. Characterization of a Ralstonia solanacearum operon required for polygalacturonate degradation and uptake of galacturonic acid. Mol. Plant-Microbe Interact. 16:536-544. (Pubitemid 36610725)
28. Hayward, A. C. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65-87.
29. Henderson, B., Wilson, M., McNab, R., and Lax, A. J. 1999. Cellular Microbiology. Bacteria-Host Interactions in Health and Disease. John Wiley and Sons, New York.
30. Hendrick, C, and Sequeira, L. 1984. Lipopolysaccharide-defective mutants of the wilt pathogen Pseudomonas solanacearum. Appl. Environ. Microbiol. 48:94-101. (Pubitemid 14052780)
31. Hikichi, Y, Yoshimochi, T, Tsujimoto, S., Shinohara, R., Nakaho, K., Kanda, A., Kiba, A., and Ohnishi, K. 2007. Global regulation of pathogenicity mechanism of Ralstonia solanacearum. Plant Biotechnol. 24:149-154. (Pubitemid 46475108)
32. Huynh, T. V, Dahlbeck, D., and Staskawicz, B. J. 1989. Bacterial blight of soybean: Regulation of a pathogen gene determining host cultivar specificity. Science 245:1374-1377.
33. Jang, J. H., Hia, H. C, Ike, M., Inoue, C, Fujita, M., and Yoshida, T. 2005. Acid hydrolysis and quantitative determination of total hexosamines of an exopolysaccharide produced by Citrobacter spp. Biotechnol. Lett. 27:13-18. (Pubitemid 40252789)
34. Janse, J. D., van den Beld, H. E., Elphinstone, J., Simpkins, S., Tjou-Tam-Sin, N. A. A., and van Vaerenbergh, J. 2004. Introduction to Europe of Ralstonia solanacearum biovar 2, race 3 in pelargonium zonale cuttings. J. Plant Pathol. 86:147-155. (Pubitemid 39160907)
35. Kachlany, S. C, Planet, P. J., Bhattacharjee, M. K., Kollia, E., DeSalle, R., Fine, D. H., and Figurski, D. H. 2000. Nonspecific adherence of Actino-bacillus actinomycetemcomitans requires genes widespread in bacteria and archaea. J. Bacteriol. 182:6169-6176.
36. Kachlany, S. C, Planet, P. J., DeSalle, R., Fine, D. H., Figurski, D. H., and Kaplan, J. 2001. flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actino-mycetemcomitans. Mol. Microbiol. 40:542-554. (Pubitemid 32453109)
37. Kang, Y., Huang, J. Z., Mao, G. Z., He, L. Y., and Schell, M. A. 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. (Pubitemid 2105556)
38. Kang, Y, Liu, H., Genin, S., Schell, M. A., and Denny, P. T. 2002. Ralstonia solanacearum requires type IV pili to adhere to multiple surfaces and for natural transformation and virulence. Mol. Microbiol. 2:427-437. (Pubitemid 35340954)
39. Kelman, A. 1954. The relationship of pathogenicity in Pseudomonas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 44:693-695.
40. Kram, K. E., Hovel-Miner, G. A., Tomich, M., and Figurski, D. H. 2008. Transcriptional regulation of the tad locus in Aggregatibacter actinomy-cetemcomitans: A termination cascade. J. Bacteriol. 190:3859-3868. (Pubitemid 351732864)
41. Liu, H., Kang, Y, Genin, S., Schell, M. A., and Denny, T. P. 2001. Twitching motility of Ralstonia solanacearum requires a type IV pilus system. Microbiology 147:3215-3229. (Pubitemid 33150328)
42. Liu, H., Zhang, S., Schell, M. A., and Denny, T. P. 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. (Pubitemid 41682601)
43. Mattick, J. S., Whitchurch, C. B., and Alm, R. A. 1996. The molecular genetics of type IV fimbriae in Pseudomonas aeruginosa. Gene 179:147-155. (Pubitemid 26395088)
44. McGarvey, J. A., Denny, T. P., and Schell, M. A. 1999. Spatial-temporal and quantitative analysis of growth and EPS production by Ralstonia solanacearum in resistant and susceptible tomato cultivars. Phytopathology 89:1233-1239.
45. 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, NY, U.S.A.
46. Morris, C. E., and Monier, J. M. 2003. The ecological significance of biofilm formation by plant-associated bacteria. Annu. Rev. Phytopathol. 41:429-453. (Pubitemid 37399689)
47. Nika, J. R., Latimer, J. L., Ward, C. K., Blick, R. J., Wagner, N. J., Cope, L. D., Mahairas, G. G., Munson, R. S., and Hansen, E. J. 2002. Haemophilus ducreyi requires the flp gene cluster for microcolony formation in vitro. Infect. Immun. 70:2965-2975. (Pubitemid 34564155)
48. O'Toole, G. A., and Kolter, R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304. (Pubitemid 28480181)
49. Pelicic, V 2008. Type IV pili: E pluribus unum? Mol. Microbiol. 68:827-837. (Pubitemid 351596335)
50. Perez, B. A., Planet, P. J., Kachlany, S. C, Tomich, M., Fine, D. H., and Figurski, D. H. 2006. Genetic analysis of the requirement for flp-2, tadV, and rcpB in Actinobacillus actinomycetemcomitans biofilm formation. J. Bacteriol. 188:6361-6375. (Pubitemid 44448579)
51. Planet, P. J., Kachlany, S. C, DeSalle, R., and Figurski, D. H. 2001. Phy-logeny of genes for secretion NTPases: Identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. U.S.A. 98:2503-2508. (Pubitemid 32209511)
52. Planet, P. J., Kachlany, S. C, Fine, D. H., DeSalle, R., and Figurski, D. H. 2003. The widespread colonization island of Actinobacillus actinomycetemcomitans. Nat. Genet. 34:193-198. (Pubitemid 36666931)
53. Possot, O., and Pugsley, A. P. 1994. Molecular characterization of PulE, a protein required for pullulanase secretion. Mol. Microbiol. 12:287-299.
54. Poueymiro, M., and Genin, S. 2009. Secreted proteins from Ralstonia solanacearum: A hundred tricks to kill a plant. Curr. Opin. Microbiol. 12:44-52.
55. Prior, P., Bart, S., Leclercq, S., Darrasse, A., and Anais, G 1996. Resistance to bacterial wilt in tomato as discerned by spread of Pseudomonas (Burk-holderia) solanacearum in the stem tissues. Plant Pathol. 45:720-726. (Pubitemid 27103201)
56. Salanoubat, M., Genin, S., Artiguenave, F, Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J., Cattolico, L., Chandler, M., Choisne, N., Claudel-Renard, C, Cunnac, S., Demange, N., Gaspin, C, Lavie, M., Moisan, A., Robert, C, Saurin, W., Schiex, T, Siguier, P., Thebault, P., Whalen, M., Wincker, P., Levy, M., Weissenbach, J., and Boucher, C. A. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502. (Pubitemid 34130598)
57. Sambrook, J., and Russel, D. W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
58. Schell, M. A. 2000. Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 38:263-292.
59. Schreiner, H. C, Sinatra, K., Kaplan, J. B., Furgang, D., Kachlany, S. C, Planet, P. J., Perez, B. A., Figurski, D. H., and Fine, D. H. 2003. Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc. Natl. Acad. Sci. U.S.A. 100:7295-7300. (Pubitemid 36706432)
60. Smith, J. J. 2003. Towards the development of a biofilm-specific expression system: Effects of different promoters, gene dosage and growth phases on extracellular expression of Pseudomonas aeruginosa DSM1707 alkaline protease. M.Sc. thesis, Department of Microbiology and Plant Pathology, University of Pretoria, South Africa.
61. Spinola, S. M., Fortney, K. R., Katz, B. P., Latimer, J. L., Mock, J. R., Vakevainen, M., and Hansen, E. J. 2003. Haemophilus ducreyi requires an intact flp gene cluster for virulence in humans. Infect. Immun. 71:7178-7182. (Pubitemid 37475353)
62. Stemmer, W. P. C, and Sequeira, L. 1987. Fimbriae of phytopathogenic and symbiotic bacteria. Phytopathology 77:1633-1639.
63. Swanson, J. K., Yao, J., Tans-Kersten, J. K., and Allen, C. 2005. Behavior of Ralstonia solanacearum race 3 biovar 2 during latent and active infection of geranium. Phytopathology 95:136-143.
64. Tans-Kersten, J., Huang, H. Y, and Allen, C. 2001. Ralstonia solanacearum needs motility for invasive virulence on tomato. J. Bacteriol. 183:3597-3605. (Pubitemid 32510427)
65. Tomich, M., Fine, D. H., and Figurski, D. H. 2006. The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J. Bacteriol. 188:6899-6914. (Pubitemid 44497903)
66. Tomich, M., Planet, P. J., and Figurski, D. H. 2007. The tad locus: Postcards from the widespread colonization island. Nat. Rev. Microbiol. 5:363-375. (Pubitemid 46605490)
67. 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. (Pubitemid 30229473)
68. Vasse, J., Frey, P., and Trigalet, A. 1995. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 8:241-251.
69. Vasse, J., Danoun, S., and Trigalet, A. 2005. Microscopic studies of root infection in resistant tomato cultivar Hawaii 7996. Pages 285-291 in: Bacterial Wilt Disease and the Ralstonia solanacearum Species Complex. C. Allen, P. Prior, and A. C. Hayward, eds. American Phytopa-thological Society, St. Paul, MN, U.S.A.
70. Wall, D., and Kaiser, D. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:1-10. (Pubitemid 29167183)
71. Wang, Y, and Chen, C. 2005. Mutation analysis of the flp operon in Actinobacillus actinomycetemcomitans. Gene 351:61-71. (Pubitemid 40732620)
72. Whitchurch, C. B., Hobbs, M., Livingston, S. P., Krishnapillai, V, and Mattick, J. S. 1991. Characterization of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialized protein export system widespread in eubacteria. Gene 101:33-44.
73. Williamson, L., Hudelson, B. D., and Allen, C. 2002. Ralstonia solanacearum strains isolated from geranium belong to Race 3 and are pathogenic on potato. Plant Dis. 86:987-991.
74. Yao, J., and Allen, C. 2006. Chemotaxis is required for virulence and competitive fitness in the bacterial wilt pathogen Ralstonia solanacearum. J. Bacteriol. 188:3697-3708. (Pubitemid 43726232)
75. Yao, J., and Allen, C. 2007. The plant pathogen Ralstonia solanacearum needs aerotaxis for normal biofilm formation and interactions with its tomato host. J. Bacteriol. 189:6415-6424. (Pubitemid 47378650)