Bacterial type two secretion system secreted proteins: Double-edged swords for plant pathogens

Molecular Plant-Microbe Interactions

Volumn 18, Issue 9, 2005, Pages 891-898

  Jha, Gopaljee ^a   Rajeshwari, R ^a   Sonti, Ramesh V ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

Cell wall degrading enzymes; Phytopathogenic bacteria; Programmed cell death; Pseudopilus; Sec dependent pathway

Indexed keywords

BACTERIAL PROTEIN;

BACTERIAL GENE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; BIOLOGICAL MODEL; GENETICS; MICROBIOLOGY; MULTIGENE FAMILY; PATHOGENICITY; PHYSIOLOGY; PLANT; PLANT DISEASE; REVIEW; VIRULENCE;

BACTERIA; BACTERIAL PHYSIOLOGY; BACTERIAL PROTEINS; GENES, BACTERIAL; MODELS, BIOLOGICAL; MULTIGENE FAMILY; PLANT DISEASES; PLANTS; VIRULENCE;

NEGIBACTERIA;

EID: 23844536513     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-18-0891     Document Type: Review

References (84)

1. Abramovitch, R. B., and Martin, G. B. 2004. Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 7:356-364.
2. Andro, T., Chambost, J.-P., Kotoujansky, A., Cattaneo, J., Bertheau, Y., Barras, F., van Gijsegem, F., and Coleno, A. 1984. Mutants of Erwinia chrysanthemi defective in secretion of pectinase and cellulase. J. Bacteriol. 160:1199-1203.
3. Ast, V. M., Schoenhofen, I. C., Langen, G. R., Stratilo, C. W., Chamberlain, M. D., and Howard, S. P. 2002. Expression of the ExeAB complex of Aeromonas hydrophila is required for the localization and assembly of the ExeD secretion port multimer. Mol. Microbiol. 44:217-231.
4. Ball, G., Durand, E. Lazdunski, A., and Filloux, A. 2002. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43:475-485.
5. Barber, C. E., Tang, J. L., Feng, J. X., Pan, M. Q., Wilson, T. J. G., Slater, H., Dow, J. M., Williams, P., and Daniels, M. J. 1997. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol. Microbiol. 24:555-566.
6. Barras, F., van Gijsegem, F., and Chatterjee, A. K. 1994. Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu. Rev. Phytopathol. 32:201-234.
7. Bell, K. S., Sebaihia, M., Pritchard, L., Holden, M. T., Hyman, L. J., Holeva, M. C., Thomson, N. R., Bentley, S. D., Churcher, L. J., Mungal, K., Atkin, R., Bason, N., Brooks, K., Chillingworth, T., Clark, K., Doggett, J., Fraser, A., Hance, Z., Hauser, H., Jagels, K., Moule, S., Norbertczak, H., Ormond, D., Price, C., Quail, M. A., Sanders, M., Walker, D., Whitehead, S., Salmond, G. P., Birch, P. R., Parkhill, J., and Toth, I. K. 2004. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. U.S.A. 101:11105-11110.
8. Braun, E. J., and Rodrigues, C. A. 1993. Purification and properties of an endoxylanase from a corn stalk rot strain of Erwinia chrysanthemi. Phytopathology 83:332-338.
9. Buell, C. R., Joardar, V., Lindeberg, M., Selengut, J., Paulsen, I. T., Gwinn, M. L., Dodson, R. J., Deboy, R. T., Durkin, A. S., Kolonay, J. F., Madupu, R., Daugherty, S., Brinkac, L., Beanan, M. J., Haft, D. H., Nelson, W. C., Davidsen, T., Zafar, N., Zhou, L., Liu, J., Yuan, Q., Khouri, H., Fedorova, N., Tran, B., Russell, D., Berry, K., Utterback, T., Van Aken, S. E., Feldblyum, T. V., D'Ascenzo, M., Deng, W. L., Ramos, A. R., Alfano, J. R., Cartinhour, S., Chatterjee, A. K., Delaney, T. P., Lazarowitz, S. G., Martin, G. B., Schneider, D. J., Tang, X., Bender, C. L., White, O., Fraser, C. M., and Collmer, A. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 100:10181-10186.
10. Condemine, G., Dorel, C., Hogouvieux-Cotte-Pattat, N., and Robert-Baudouy, J. 1992. Some of the out genes involved in the secretion of pectate lyases in Erwinia chrysanthemi are regulated by kdgR. Mol. Microbiol. 6:3199-3211.
11. Corbett, M., Virtue, S., Bell, K., Birch, P., Burr, T., Hyman, L., Lilley, K., Poock, S., Toth, I., and Salmond, G. 2005. Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol. Plant-Microbe Interact. 18:334-342.
12. Darvill, A. G., and Albersheim, P. 1984. Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu. Rev. Plant Physiol. 35:243-275.
13. da Silva, A. C., Ferro, J. A., Reinach, F. C., Farah, C. S., Furlan, L. R., Quaggio, R. B., Monteiro-Vitorello, C. B., Van Sluys, M. A., Almeida, N. F., Alves, L. M, do Amaral, A. M., Bertolini, M. C., Camargo, L. E., Camarotte, G., Cannavan, F., Cardozo, J., Chambergo, F., Ciapina, L. P., Cicarelli, R. M., Coutinho, L. L., Cursino-Santos, J. R., El-Dorry, H., Faria, J. B., Ferreira, A. J., Ferreira, R. C., Ferro, M. I., Formighieri, E. F., Franco, M. C., Greggio, C. C., Gruber, A., Katsuyama, A. M., Kishi, L. T., Leite, R. P., Lemos, E. G., Lemos, M. V., Locali, E. C., Machado, M. A., Madeira, A. M., Martinez-Rossi, N. M., Martins, E. C., Meidanis, J., Menck, C. F., Miyaki, C. Y., Moon, D. H., Moreira, L. M., Novo, M. T., Okura, V. K., Oliveira, M. C., Oliveira, V. R., Pereira, H. A., Rossi, A., Sena, J. A., Silva, C., de Souza, R. F., Spinola, L. A., Takita, M. A., Tamura, R. E., Teixeira, E. C., Tezza, R. I., Trindade dos Santos, M., Truffi, D., Tsai, S. M., White, F. F, Setubal, J. C., and Kitajima, J. P. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-463.
14. Dow, J. M., Scofield, G., Trafford, K., Turner, P. C., and Daniels, M. J. 1987. A gene cluster in Xanthomonas campestris pv. campestris required for pathogenicity controls the excretion of polygalacturonate lyase and other enzymes. Physiol. Mol. Plant Pathol. 31:261-271.
15. Dow, J. M., Daniels, M. J., Dums, F., Turner, P. C., and Cough, C. 1989a. Genetic and biochemical analysis of protein export from Xanthomonas campestris. J. Cell Sci. (Suppl.) 11:59-72.
16. Dow, J. M., Milligan, D. E., Jamieson, L., Barber, C. E., and Daniels, M. J. 1989b. Molecular cloning of a polygalacturonate lyase gene from Xanthomonas campestris pv. campestris and role of the gene product in pathogenicity. Physiol. Mol. Plant Pathol. 35:113-120.
17. Dow, J. M., Clarke, B. R., Milligan, D. E., Tang, J.-L., and Daniels, M. J. 1990. Extracellular proteases from Xanthomonas campestris pv. campestris, the black rot pathogen. Appl. Environ. Microbiol. 56:2994-2998.
18. Dums, F., Dow, J. M., and Daniels, M. J. 1991. Structural characterization of protein secretion genes of the bacterial phytopathogen Xanthomonas campestris pathovar campestris: Relatedness to secretion systems of other gram-negative bacteria. Mol. Gen. Genet. 229:357-364.
19. Durand, E., Bernadac, A., Ball, G., Lazdunski, A., Sturgis, J. N., and Filloux, A. 2003. Type II protein secretion in Pseudomonas aeruginosa: The Pseudopilus is a multifibrillar and adhesive structure. J. Bacteriol. 185:2749-2758.
20. Enkerli, J., Felix, G., and Boller, T. 1999. The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol. 121:391-397.
21. 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 system. Mol. Plant-Microbe Interact. 8:845-854.
22. Filloux, A. 2004. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694:163-179.
23. Filloux, A., Michel, G., and Bally, G. 1998. GSP-dependent protein secretion in gram-negative bacteria: The Xcp system of Pseudomonas aeruginosa. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 22:177-198.
24. Furutani, A., Tsuge, S., Ohnishi, K., Hikichi, Y., Oku, T., Tsuno, K., Inoue, Y., Ochiai, H., Kaku, H., and Kubo, Y. 2004. Evidence for HrpXo-dependent expression of type II secretory proteins in Xanthomonas oryzae pv. oryzae. J. Bacteriol. 186:1374-1380.
25. Goodner, B., Hinkle, G., Gattung, S., Miller, N., Blanchard, M., Qurollo, B., Goldman, B. S., Cao, Y., Askenazi, M., Halling, C., Mullin, L., Houmiel, K., Gordon, J., Vaudin, M., Iartchouk, O., Epp, A., Liu, F., Wollam, C., Allinger, M., Doughty, D., Scott, C., Lappas, C., Markelz, B., Flanagan, C., Crowell, C., Gurson, J., Lomo, C., Sear, C., Strub, G., Cielo, C., Slater, S. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323-2328.
26. Gough, C. L., Dow, J. M., Barber, C. E., and Daniels, M. J. 1988. Cloning of two endoglucanase genes of Xanthomonas campestris pv. campestris: Analysis of the role of the major endoglucanase in pathogenesis. Mol. Plant-Microbe Interact. 1:275-281.
27. Govrin, E. M., and Levine, A. 2000. The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10:751-757.
28. Hardie, K. R., Lory, S., and Pugsley, A. P. 1996. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO (Eur. Mol. Biol. Organ.) J. 15:978-988.
29. He, S. Y., Lindeberg, M., Chatterjee, A. K., and Collmer, A. 1991. Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc. Natl. Acad. Sci. U.S.A. 88:1079-1083.
30. Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C., and Ala'Aldeen, D. 2004. Type V protein secretion pathway: The autotransporter story. Microbiol. Mol. Biol. Rev. 68:692-744.
31. Hinton, J. C. D., Sidebotham, J. M., Hyman, L. J., Perombelon, M. C. M., and Salmond, G. P. C. 1989. Isolation and characterization of transposon-induced mutants of Erwinia carotovora subsp. atroseptica exhibiting reduced virulence. Mol. Gen. Genet. 217:141-148.
32. Hu, N.-T., Hung, M.-N, Chiou, S.-J., Tang, F., Chiang, D.-C., Huang, H.-Y., and Wu, C.-Y. 1992. Cloning and characterization of a gene required for the secretion of extracellular enzymes across the outer membrane by Xanthomonas campestris pv. campestris. J. Bacteriol. 174:2679-2687.
33. Hu, N.-T., Lee, P.-F., and Chen, C. 1995. The type IV pre-pilin leader peptidase of Xanthomonas campestris pv. campestris is functional without conserved cysteine residues. Mol. Microbiol. 18:769-777.
34. Huang, Q., and Allen, C. 1997. An exo-poly-α-D-galacturonosidase, PehB, is required for wild-type virulence of Ralstonia solanacearum. J. Bacteriol. 179:7369-7378.
35. Jha, G., Rajeshwari, R., and Sonti, R. V. 2004. Abstract KA3. The Ist Int. Conf. Bacterial Blight of Rice, Tsukuba, Japan
36. Kang, Y., Huang, J., Mao, G., He, L., 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.
37. Kariola, T., Palomäki, T. A., Brader, G., and Palva, E. T. 2003. Erwinia carotovora subsp. carotovora and Erwinia-derived elicitors HrpN and PehA trigger distinct but interacting defense responses and cell death in Arabidopsis. Mol. Plant-Microbe Interact. 16:179-187.
38. Kazemi-Pour, N., Condemine, G., and Hugouvieux-Cotte-Pattat, N. 2004. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4:3177-3186.
39. Kelemu, S., and Collmer, A. 1993. Erwinia chrysanthemi EC16 produces a second set of plant-inducible pectate lyase isozymes. Appl. Environ. Microbiol. 59:1756-1761.
40. Kita, N., Boyd, C. M, Garrett, M. R., Jurnak, F., and Keen, N. T. 1996. Differential effect of site-directed mutations in pelC on pectate lyase activity, plant tissue maceration, and elicitor activity. J. Biol. Chem. 271:26529-26535.
41. Laatu, M., and Condemine, G. 2003. Rhamnogalacturonate lyase RhiE is secreted by the Out system in Erwinia chrysanthemi. J. Bacteriol. 185:1642-1649.
42. 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. 2005a. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 33:577-586.
43. Lee, M.-S., Chen, L.-Y., Leu, W.-M., Shiau, R.-J., and Hu, N.-T. 2005b. Associations of the major Pseudopilin XpsG with XpsN (GspC) and secretin XpsD of Xanthomonas campestris pv. campestris type II secretion apparatus revealed by cross-linking analysis. J. Biol. Chem. 280:4585-4591.
44. Lindeberg, M., and Collmer, A. 1992. Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: Sequence comparison with secretion genes from other gram-negative bacteria, J. Bacteriol. 174:7385-7397.
45. Murata, H., Fons, M., Chatterjee, A., Collmer, A., and Chatterjee, A. K. 1990. Characterization of transposon insertion Out mutants of Erwinia carotovora subsp. carotovora defective in enzyme export and of a DNA segment that complements out mutations in E. carotovora subsp. carotovora, E. carotovora subsp. atroseptica, and Erwinia chrysanthemi. J. Bacteriol. 172:2970-2978.
46. Norman, C., Vidal, S., and Palva, E. T. 1999. Oligogalacturonide-mediated induction of a gene involved in jasmonic acid synthesis in response to the cell-wall-degrading enzymes of the plant pathogen Erwinia carotovora. Mol. Plant-Microbe Interact. 12:640-644.
47. Norman-Setterblad, C., Vidal, S., and Palva, E. T. 2000. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora. Mol. Plant-Microbe Interact. 13:430-438.
48. Palva, T. K., Holmstrom, K.-O., Heino, P., and Palva, E. T. 1993. Induction of plant defense response by exoenzymes of Erwinia carotovora subsp. carotovora. Mol. Plant-Microbe Interact. 6:190-196.
49. Parker, J. E., Barber, C. E., Fan, M. J., and Daniels, M. J. 1993. Interaction of Xanthomonas campestris with Arabidopsis thaliana: Characterization of a gene from X. c. pv. raphani that confers avirulence to most A. thaliana accessions. Mol Plant-Microbe Interact. 6:216-224.
50. Peabody, C. R., Chung, Y. J., Yen, M.-R., Vidal-Ingigliardi, D., Pugsley, A. P., and Saier, M. H., Jr. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
51. Pirhonen, M., Saarilahti, H. T., Karlsson, M. B., and Palva, E. T. 1991. Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol. Plant-Microbe Interact. 4:276-283.
52. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
53. Py, B., Barras, F., Harris, S., Robson, N., and Salmond, G. P. C. 1998. Extracellular enzymes and their role in Erwinia virulence. Methods Microbiol. 27:157-168.
54. Py, B., Loiseau, L., and Barras, F. 2001, An inner membrane platform in the type II secretion machinery of gram-negative bacteria. EMBO (Eur. Mol. Biol. Organ.) Rep. 2:244-248.
55. 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.
56. Ray, S. K., Rajeshwari, R., and Sonti, R. V. 2000. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol. Plant-Microbe Interact. 13:394-401.
57. Reeves, P. J., Whitcombe, D., Wharam, S., Gibson, M., Allison, G., Bunce, N., Barallon, R., Douglas, P., Mulholland, V., Stevens, S., Walker, D., and Salmond, G. P. C. 1993. Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: Genes encoding members of a general secretion pathway (GSP) widespread in gram-negative bacteria. Mol. Microbiol. 8:443-456.
58. Reimers, P. J., and Leach, J. E. 1991. Race-specific resistance to Xanthomonas oryzae pv. oryzae conferred by bacterial blight resistance gene Xa-10 in rice (Oryza sativa) involves accumulation of a lignin-like substance in host tissues. Physiol. Mol. Plant Pathol. 38:39-55.
59. Ried, J. L., and Collmer, A. 1988. Construction and characterization of an Erwinia chrysanthemi mutant with directed deletions in all of the pectate lyase structural genes. Mol. Plant-Microbe Interact. 1:32-38.
60. Roberts, D. P., Denny, T. P., and Schell, M. A. 1988. Cloning of the egl gene of Pseudomonas solanacearum and analysis of its role in phytopathogenicity. J. Bacteriol. 170:1445-1451.
61. Roine, E., Raineri, D. M., Romantschuk, M., Wilson, M., and Nunn, D. N. 1998. Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 11:1048-1056.
62. Ron, M., and Avni, A. 2004. The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 10:1604-1615.
63. Rotblat, B., Enshell-Seijiffers, D., Gershoni, J. M., Schuster, S., and Avni, A. 2002. Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J. 32:1049-1055.
64. Ryan, C. A., and Farmer, E. E. 1991. Oligosaccharide signals in plants: A current assessment. Annu. Rev. Plant Physiol. Mol. Biol. 42:651-674.
65. Salanoubat, M., Genin, S., Artiguenave, F., Gouzy, J., Mangenot, S., Arlat, M., Billault, A., Brottier, P., Camus, J. C., 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., Wineker, P., Levy, M., Weissenbach, J., and Boucher, C. A. 2002. Genome sequence of the plant pathogen Ralstonia solanaceaum. Nature 415:497-502.
66. Sandkvist, M. 2001a. Biology of type II secretion. Mol. Microbiol. 40:271-283.
67. Sandkvist, M. 2001b. Type II secretion and pathogenesis. Infect. Immun. 69:3523-3535.
68. Sauvonnet, N., Vignon, G., Pugsley, A. P., and Gounon, P. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO (Eur. Mol. Biol. Organ.) J. 19:2221-2228.
69. Schell, M. A. 2000. Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 38:263-292.
70. Shevchik, V. E., Robert-Baudouy, J., and Condemine, G. 1997. Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO (Eur. Mol. Biol. Organ.) J. 16:3007-3016.
71. Shevchik, V. E., Boccara, M., Vedel, R., and Hugouvieux-Cotte-Pattat, N. 1998. Processing of the pectate lyase Pell by extracellular proteases of Erwinia chrysanthemi 3937. Mol. Microbiol. 29:1459-1469.
72. Simpson, A. J., Reinach, F. C., Arruda, P., Abreu, F. A., Acencio, M., Alvarenga, R., Alves, L. M., Araya, J. E., Baia, G. S., Baptista, C. S., Barros, M. H., Bonaccorsi, E. D., Bordin, S., Bove, I. M., Briones, M. R., Bueno, M. R., Camargo, A. A., Camargo, L. E., Carraro, D. M., Carrer, H., Colauto, N. B., Colombo, C., Costa, F. F., Costa, M. C., Costa-Neto, C. M., Coutinho, L. L., Cristofani, M., Dias-Neto, E., Docena, C., El-Dorry, H., Facincani, A. P., Ferreira, A. J., Ferreira, V. C., Ferro, J. A., Fraga, J. S., Franca, S. C., Franco, M. C., Frohme, M., Furlan, L. R., Garnier, M., Goldman, G. H., Goldman, M. H., Gomes, S. L., Gruber, A., Ho, P. L., Hoheisel, J. D., Junqueira, M. L., Kemper, E. L., Kitajima, J. P., Krieger, J. E., Kuramae, E. E., Laigret, F., Lambais, M. R., Leite, L. C., Lemos, E. G., Lemos, M. V., Lopes, S. A., Lopes, C. R., Machado, J. A., Machado, M. A., Madeira, A. M., Madeira, H. M., Marino, C. L., Marques, M. V., Martins, E. A., Martins, E. M., Matsukuma, A. Y., Menck, C. F., Miracca, E. C., Miyaki, C. Y., Monteriro-Vitorello, C. B., Moon, D. H., Nagai, M. A., Nascimento, A. L., Netto, L. E., Nhani, A. Jr, Nobrega, F. G., Nunes, L. R., Oliveira, M. A., de Oliveira, M. C., de Oliveira, R. C., Palmieri, D. A., Paris, A., Peixoto, B. R., Pereira, G. A., Pereira, H. A. Jr., Pesquero, J. B., Quaggio, R. B., Roberto, P. G., Rodrigue,s V., de M Rosa, A. J., de Rosa, V. E. Jr., de Sa, R. G., Santelli, R. V., Sawasaki, H. E., da Silva, A. C., da Silva, A. M., da Silva, F. R., da Silva, W. A. Jr., da Silveira, J. F., Silvestri, M. L., Siqueira, W. J., de Souza, A. A., de Souza, A. P., Terenzi, M. F., Truffi, D., Tsai, S. M., Tsuhako, M. H., Vallada, H., Van Sluys, M. A., Verjovski-Almeida, S., Vettore, A. L., Zago, M. A., Zatz, M., Meidanis, J., and Setubal, J. C. 2000. The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406:151-157.
73. Strom, M. S., Nunn, D., and Lory, S. 1991. Multiple roles of the pilus biogenesis protein PilD: Involvement of PilD in excretion of enzymes from Pseudomonas aeruginosa. J. Bacteriol. 173:1175-1180.
74. Sun, Q. H., Hu, J., Huang, G. X., Ge, C., Fang, R. X., and He, C. Z. 2005. Type-II secretion pathway structural gene xpsE, xylanase, and cellulase secretion and virulence in Xanthomonas oryzae pv. oryzae. Plant Pathol. 54:15-21.
75. Thomson, N. R., Thomas, J. D., and Salmond, G. P. C. 1999. Virulence determinants in the bacterial phytopathogen Erwinia. Methods Microbiol. 29:347-426.
76. Thurn, K. K., and Chatterjee, A. K. 1985. Single-site chromosomal Tn5 insertions affect the export of pectolytic and cellulolytic enzymes in Erwinia chrysanthemi EC16. Appl. Environ. Microbiol. 50:894-898.
77. Vidal, S., Eriksson, A. R. B., Montesano, M., Denecke, J., and Palva, E. T. 1998. Cell wall-degrading enzymes from Erwinia carotovora cooperate in the salicylic acid-independent induction of a plant defense response. Mol. Plant-Microbe Interact. 11:23-32.
78. Voulhoux, R., Ball, G., Ize, B., Vasil, M. L., Lazdunski, A., Wu, L. F., and Filloux, A. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO (Eur. Mol. Biol. Organ.) J. 20:6735-6741.
79. Wang, L. H., He, Y. W., Gao, Y. F., Wu, J. E., Dong, Y. H., He, C. Z., Wang, S. X., Weng, X., Xu, J. L., Tay, L., Fang, R. X., and Zhang, L. H. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51:903-912.
80. Wegener, C., Bartling, S., Olsen, O., Weber, J., and van Wettstein, D. 1996. Pectate lyase in transgenic potatoes confers pre-activation of defence against Erwinia carotovora. Physiol. Mol. Plant Pathol. 49:359-376.
81. Wood, D. W., Setubal, J. C., Kaul, R., Monks, D. E., Kitajima, J. P., Okura, V. K., Zhou, Y., Chen, L., Wood, G. E., Almeida, N. F. Jr., Woo, L., Chen, Y., Paulsen, I. T., Eisen, J. A., Karp, P. D., Bovee, D. Sr., Chapman, P., Clendenning, J., Deatherage, G., Gillet, W., Grant, C., Kutyavin, T., Levy, R., Li, M. J., McClelland, E., Palmieri, A., Raymond, C., Rouse, G., Saenphimmachak, C., Wu, Z., Romero, P., Gordon, D., Zhang, S., Yoo, H., Tao, Y., Biddle, P., Jung, M., Krespan, W., Perry, M., Gordon-Kamm, B., Liao, L., Kim, S., Hendrick, C., Zhao, Z. Y., Dolan, M., Chumley, F., Tingey, S. V., Tomb, J. F., Gordon, M. P., Olson, M. V., and Nester, E. W. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317-2323.
82. Whitehead, N. A., Barnard, A. M. L., Slater, H., Simpson, N. J. L., and Salmond, G. P. C. 2001. Quorum-sensing in gram-negative bacteria. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 25:365-404.
83. Whitehead, N. A., Byers, J. T., Commander, P., Corbett, M. J., Coulthurst, S. J., Everson, L., Harris, A. K. P., Pemberton, C. L., Simpson, N. J. L., Slater, H., Smith, D. S., Welch, M., Williamson, N., and Salmond, G. P. C. 2002. The regulation of virulence in phytopathogenic Erwinia species: Quorum sensing, antibiotics and ecological considerations. Antonie Leeuwenhoek 81:223-231.
84. Yang, B., Zhu, W., Johnson, L. B., and White, F. F. 2000. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway- dependent nuclear-localized double-stranded DNA binding protein. Proc. Natl. Acad. Sci. U.S.A. 97:9807-9812.