XadM, a novel adhesin of Xanthomonas oryzae pv. oryzae, exhibits similarity to Rhs family proteins and is required for optimum attachment, biofilm formation, and virulence

Molecular Plant-Microbe Interactions

Volumn 25, Issue 9, 2012, Pages 1157-1170

  Pradhan, Binod B ^a   Ranjan, Manish ^a   Chatterjee, Subhadeep ^a  

^a CENTRE FOR DNA FINGERPRINTING AND DIAGNOSTICS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN;

ARTICLE; BACTERIUM ADHERENCE; BIOFILM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; RICE; VIRULENCE; XANTHOMONAS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; ORYZA SATIVA; PLANT DISEASES; VIRULENCE; XANTHOMONAS;

ANIMALIA; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); BURKHOLDERIA; XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZAE;

EID: 84864676576     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-02-12-0049-R     Document Type: Article

References (62)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. (Pubitemid 27359211)
2. Anantharaman, V., and Aravind, L. 2003. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4:R11. Published online.
3. Blake, M. S., Blake, C. M., Apicella, M. A., and Manderell, R. E. 1995. Gonococcal opacity: Lectin-like interactions between opa proteins and lipooligosaccharide. Infect. Immun. 63:1434-1439.
4. Buddelmeijer, N., Aarsman, M. E. G., Kolk, A. H. J., Vicente, M., and Nanninga, N. 1998. Localization of cell division protein FtsQ by Immunofluorescence microscopy in dividing and nondividing cells of Escherichia coli. J. Bacteriol. 180:6107-6116. (Pubitemid 28544240)
5. Büttner, D., and Bonas, U. 2010. Regulation and secretion of Xanthomonas virulence factors. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 34:107-133.
6. Chatterjee, S., and Sonti, R. V. 2002. rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. Mol. Plant-Microbe Interact. 15:463-471. (Pubitemid 34523132)
7. Chatterjee, S., Sankaranarayanan, R., and Sonti, R. V. 2003. PhyA, a secreted protein of Xanthomonas oryzae pv. oryzae, is required for optimum virulence and growth on phytic acid as a sole phosphate source. Mol. Plant-Microbe Interact. 16:973-982. (Pubitemid 37325643)
8. Chatterjee, S., Wistrom, C., and Lindow, S. E. 2008. A cell-cell signaling sensor is required for virulence and insect transmission of X. fastidiosa. Proc. Natl. Acad. Sci. U. S. A. 105:2670-2675. (Pubitemid 351520571)
9. Chatterjee, S., Killiny, N., Almeida, R. P. P., and Lindow S. E. 2010. Role of cyclic di-GMP in Xylella fastidiosa biofilm formation, plant virulence, and insect transmission. Mol. Plant-Microbe Interact. 23:1356-1363.
10. Danhorn T., and Fuqua C. 2007. Biofilm formation by plant-associated bacteria. Annu. Rev. Microbiol. 61:401-422. (Pubitemid 350058215)
11. Darsonval, A., Darrasse, A., Durand, K., Bureau, C., Cesbron, S., and Jacques, M. A. 2009. Adhesion and fitness in the bean phyllosphere and transmission to seed of Xanthomonas fuscans subsp. fuscans. Mol. Plant-Microbe Interact. 22:747-757.
12. Das, A., Rangaraj, N., and Sonti, R. V. 2009. Multiple adhesin-like functions of Xanthomonas oryzae pv. oryzae are involved in promoting leaf attachment, entry, and virulence on rice. Mol. Plant-Microbe Interact. 22:73-85.
13. DeFeyter, R., Kado, C. I., and Gabriel, D. W. 1990. Small stable shuttle vectors for use in Xanthomonas. Gene 88:65-72. (Pubitemid 20167133)
14. Dharmapuri, S., and Sonti, R. V. 1999. A transposon insertion in the gumG homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 179:53-59. (Pubitemid 29428204)
15. D'Souza, S. E., Ginsberg, M. H., Matsueda, G. R., and Plow, E. F. 1991a. A discrete sequence in a platelet integrin is involved in ligand recognition. Nature 350:66-68. (Pubitemid 21926122)
16. D'Souza, S. E., Ginsberg, M. H., and Plow, E. F. 1991b. Arginyl-glycylas-partic acid (RGD): A cell adhesion motif. Trends Biochem. Sci. 16:246-250. (Pubitemid 121004445)
17. Enos-Berlage, J. L., and McCarter, L. L. 2000. Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J. Bacteriol. 182:5513-5520.
18. Feil, H., Feil, W. S., and Lindow, S. E. 2007. Contribution of fimbrial and afimbrial adhesins of Xylella fastidiosa to attachment to surfaces and virulence to grape. Phytopathology 97:318-324. (Pubitemid 46348953)
19. Finley, B. B., and Falkow, S. 1997. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:136-169. (Pubitemid 27283798)
20. Foster, S. J. 1993. Molecular analysis of three major wall associated proteins of Bacillus subtilis 168: Evidence for processing of the product of a gene encoding a 258 kDa precursor two-domain ligand-binding protein. Mol. Microbiol. 8:299-310. (Pubitemid 23124547)
21. Goel, A. K., Rajagopal, L., and Sonti, R. V. 2001. Pigment and virulence deficiencies associated with mutations in the aroE gene of Xanthomonas oryzae pv. oryzae. Appl. Environ. Microbiol. 67:245-250. (Pubitemid 32044425)
22. Gottig, N., Garavaglia, B. S., Garofalo, C. G., Orellano, E. G., and Ottado, J. 2009. A filamentous hemagglutinin-like protein of Xanthomonas ax-onopodis pv. citri, the pathogen responsible for citrus canker, is involved in bacterial virulence. PLoS ONE 4:e4358.
23. Guilhabert, M. R., and Kirkpatrick, B. C. 2005. Identification of Xylella fastidiosa antivirulence genes: Hemagglutinin adhesins contribute to X. fastidiosa biofilm maturation and colonization and attenuate virulence. Mol. Plant-Microbe Interact. 18:856-868. (Pubitemid 41061484)
24. Hill, C. W., Sandt, C. H., and Vlazny, D. A. 1994. Rhs elements of Escherichia coli: A family of genetic composites each encoding a large mosaic protein. Mol. Microbiol. 12:865-871. (Pubitemid 24199666)
25. Jobling, M. G., and Holmes, R. K. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26:1023-1034. (Pubitemid 27507886)
26. Kauffman, H. E., Reddy, A. P. K., Hsieh, S. P. Y., and Merca, S. D. 1973. An improved technique for evaluation of resistance of rice varieties to Xanthomonas oryzae. Plant Dis. Rep. 57:537-541.
27. Kelemu, S., and Leach, J. E. 1990. Cloning and characterization of an avirulence gene from Xanthomonas campestris pv. oryzae. Mol. Plant-Microbe Interact. 3:59-65.
28. Killiny, N., and Almeida, R. P. 2009. Xylella fastidiosa afimbrial adhesions mediate cell transmission to plants by leafhopper vectors. Appl. Environ. Microbiol. 75:521-528.
29. Kung, V. L., Khare, S., Stehlik, C., Bacon, E. M., Hughes, A. J., and Hauser, A. R. 2012. An rhs gene of Pseudomonas aeruginosa encodes a virulence protein that activates the inflammasome. Proc. Natl. Acad. Sci. U. S. A. 109:1275-1280.
30. Lambden, P. R.,. Heckels, J. E., James, L. T and Watt, P. J. 1979. Variations in surface protein composition associated with virulence properties in opacity types of Neisseria gonorrhoeae. J. Gen. Microbiol. 114:305-312. (Pubitemid 10234363)
31. Lattemann, C. T., Maurer, J., Gerland, E., and Meyer, F. 2000. Autodis-play: Functional display of active blactamase on the surface of Escherichia coli by the AIDAI autotransporter. J. Bacteriol. 182:3726-3733. (Pubitemid 30413023)
32. Leach, J. E., White, F. F., Rhoads, M. L., and Leung, H. 1990. A repetitive DNA sequence differentiates Xanthomonas campestris pv. oryzae from other pathovars of X. campestris. Mol. Plant-Microbe Interact. 3:238-246.
33. Lee, B. M., Park, Y. J., Park, D. S., Kang, H. W., Kim, J. G., Song, E. S., Park, I. C., Yoon, U. H., Hahn, J. H., Koo, B. S., Lee, G. B., Kim, H., Park, H. S., Yoon, K. O., Kim, J. H., Jung, C. H., Koh, N. H., Seo, J. S., and Go, S. J. 2005. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 33:577-586. (Pubitemid 40360987)
34. Locht, C. 2007. Bordetella Molecular Biology. Horizon Bioscience, Norwich, U. K.
35. Makino, S., van Putten, J. P. M., and Meyer, T. F. 1991. Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells. EMBO (Eur. Mol. Biol. Organ.) J. 10:1307-1315. (Pubitemid 21905594)
36. McNulty, C., Thompson, J., Barrett, B., Lord, L., Andersen, C., and Roberts, I. S. 2006. The cell surface expression of group 2 capsular polysaccharide in Escherichia coli: The role of KpsD, RhsA and a multi-protein complex at the pole of the cell. Mol. Microbiol. 59:907-922.
37. Mew, T. W., Mew, I. C., and Huang, J. S. 1984. Scanning electron microscopy of virulent and avirulent strains of Xanthomonas campestris pv. oryzae on rice leaves. Phytopathology 74:635-641.
38. Minet, A. D., Rubin, B. P., Tucker, R. P., Baumgartner, S., and Chiquet-Ehrismann, R. 1999. Teneurin-1, a vertebrate homologue of the Dro-sophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J. Cell Sci. 112:2019-2032. (Pubitemid 29338826)
39. Moore, J. P., Nguema-Ona, E., Chevalier, L., Lindsey, G. G., Brandt, W. F., Lerouge, P., Farrant, J. M., and Driouich, A. 2006. Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus fla-bellifolius. Plant Physiol. 141:651-662. (Pubitemid 43974558)
40. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
41. Parsek, M. R., and Singh, P. K. 2003. Bacterial biofilms: An emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701. (Pubitemid 37392958)
42. Petersen, L., Bollback, J. P., Dimmic, M., Hubisz, M., and Nielsen, R. 2007. Genes under positive selection in Escherichia coli. Genome Res. 17:1336-1343. (Pubitemid 47360908)
43. Rajagopal, L., Jameer, Y., Dharmapuri, S., Karunakaran, M., Ramanan, R., Reddy, A. P. K., and Sonti, R. V 1995. Molecular genetic studies of the bacterial leaf blight pathogen of rice in India. Pages 939-944 in: Abstr. Rice Genetics III: Proceedings, G. S. Khush, ed. IRRI, Los Banos, The Phillipines.
44. Rajagopal, L., Dharmapuri, S., Sayeepriyadarshini, A. T., and Sonti, R. V 1999. A genomic library of Xanthomonas oryzae pv. oryzae in the board host range mobilizing Escherichia coli strain S17-1. Int. Rice Res. Notes 24:20-21.
45. Rajeshwari, R., Jha, G., and Sonti, R. V 2005. Role of an in planta-expressed xylanase of Xanthomonas oryzae pv. oryzae in promoting virulence on Rice. Mol. Plant-Microbe Interact. 18:830-837. (Pubitemid 41061481)
46. Ray, S. K., Rajeswari, R., Sharma, Y., and Sonti, R. V 2002. A high molecular weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence. Mol. Microbiol. 46:637-647. (Pubitemid 35365600)
47. Relman, D., Tuomanen, E., Falkow, S., Golenbock, D. T., Saukkonen, K., and Wright, S. D. 1990. Recognition of a bacterial adhesion by an integrin: Macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61:1375-1382.
48. Rojas, C. M., Ham, J. H., Deng, W L., Doyle, J. J., and Collmer, A. 2002. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nico-tiana clevelandii seedlings. Proc. Natl. Acad. Sci. U. S. A. 99:13142-13147.
49. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
50. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., and Puhler, A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutumicum. Gene 145:69-73. (Pubitemid 24224965)
51. Shen, Y., and Ronald, P. 2002. Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice. Microbes Infect. 4:1361-1367. (Pubitemid 35356463)
52. Simon, R., Priefer, U., and Puhler, A. 1983. A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in gram-negative bacteria. Bio/Technology 1:784-794.
53. Soto, G E., and Hultgren, S. J. 1999. Bacterial adhesins: Common themes and variations in architecture and assembly. J. Bacteriol. 181:1059-1071. (Pubitemid 29119542)
54. Stuurman, N., Bras, C. P., Schlaman, H. R. M., Wijfjes, A., Bloemberg, G., and Spaink, H. P. 2000. Use of green fluorescent protein color variants expressed on stable broad-host-range vectors to visualize rhizobia interacting with plants. Mol. Plant-Microbe Interact. 13:1163-1169.
55. Swanson, J. 1978. Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect. Immun. 21:292-302. (Pubitemid 8386112)
56. Tsuchiya, K., Mew, T. W., and Wakimoto, S. 1982. Bacteriological and pathological characteristics of wild types and induced mutants of Xanthomonas campestris pv. oryzae. Phytopathology 72:43-46.
57. Tsuge, S., Furutani, A., Fukunaka, R., Oku, T., Tsuno, K., Ochiai, H., and Inoue, Y., Kaku, H., and Kubo, Y 2002. Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J. Gen. Plant Pathol. 68:363-371.
58. Voegel, T. M., Warren, J. G., Matsumoto, A., Igo, M., and Kirkpatrick, B. C. 2010. Localization and characterization of Xylella fastidiosa hae-magglutinin adhesins. Microbiology 156:2172-2179.
59. Wei, K., Tang, D.-J., He, Y.-Q., Feng, J.-X., Jiang, B.-L., Lu, G.-T., Chen, B., and Tang, J. L. 2007. hpaR, a putative marR family transcriptional regulator, is positively controlled by HrpG and HrpX and involved in the pathogenesis, hypersensitive response, and extracellular protease production of Xanthomonas campestris pathovar campestris. J. Bacteriol. 189:2055-2062. (Pubitemid 46446169)
60. Wilson, K. J., Sessitch, A., Corbo, J. C., Giller, K. E., Akkermans, A. D. L., and Jefferson, R. A. 1995. Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other gram-negative bacteria. Microbiology 141:1691-1705.
61. Windgassen, M., Urban, A., and Jaeger, K. E..2000. Rapid gene inactiva-tion in Pseudomonas aeruginosa. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 193:201-205.
62. Zhao, S., Sandt, C. H., Feulner, G., Vlazny, D. A., Gray, J. A., and Hill, C. W. 1993. Rhs elements of Escherichia coli K-12: Complex composites of shared and unique components that have different evolutionary histories. J. Bacteriol. 175:2799-2808. (Pubitemid 23148709)