Regulation of the type III secretion system in phytopathogenic bacteria

Molecular Plant-Microbe Interactions

Volumn 19, Issue 11, 2006, Pages 1159-1166

  Tang, Xiaoyan ^a   Xiao, Yanmei ^a   Zhou, Jian Min ^b  

^a KANSAS STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL GENE; GENE EXPRESSION REGULATION; GENETICS; GRAM NEGATIVE BACTERIUM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT; PLANT DISEASE; REVIEW; VIRULENCE;

GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GRAM-NEGATIVE BACTERIA; PLANT DISEASES; PLANTS; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS SYRINGAE; RALSTONIA SOLANACEARUM;

EID: 33750208366     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-19-1159     Document Type: Review

References (85)

1. Aldon, D., Brito, B., Boucher, C., and Genin, S. 2000. A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanaceanun pathogenicity genes. EMBO (Eur. Mol. Biol. Organ.) J. 19:2304-2314.
2. Alegria, M. C., Docena, C., Khater, L., Ramos, C. H., da Silva, A. C., and Farah, C. S. 2004. New protein-protein interactions identified for the regulatory and structural components and substrates of the type 111 Secretion system of the phytopathogen Xanthomonas axonopodis pathovar citri. J. Bacteriol. 186:6186-6197.
3. Alfano, J. R., Charkowski, A. O., Deng, W. L., Badel, J. L., Petnicki-Ocwieja. T., van Dijk, K., and Collmer. A. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable-effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Nutl. Acad. Sci. U.S.A. 97:4856-4861.
4. Alfano, J. R., and Collmer, A. 1997. The type III (Hrp) secretion pathway of plain palhogenic bacleria: Trafficking harpins, Avr proteins, and death. J. Bacteriol. 179:5655-5662.
5. Arlat, M., Gough, C. L., Zischek, C., Barberis, P. A., Trigalet, A., and Boucher, C. A. 1992. Transcriptional organization and expression of the large hrp gene cluster of Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 5:187-193.
6. Arnold, D. L., Pitman, A., and Jackson, R. W. 2003. Pathogenicity and other genomic islands in plant pathogenic bacteria. Mol. Plant Pathol. 4:407-420.
7. Bender, C., Rangaswamy, V., and Loper, J. 1999. Polyketide production by plant-associated Pseudomonas. Annu. Rev. Phytopathol. 37:175-196.
8. Boch, J., Joardar, V., Gao, L., Robertson, T. L., Lim, M., and Kunkel, B. N. 2002. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44:73-88.
9. Brencic, A., and Winans, S. C. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biot. Rev. 69:155-194.
10. Bretx, J., Losuda, L., Lisboa, K., and Hutcheson, S.W. 2002. Lon protease functions as a negative regulator of type III protein secretion in Pseudomonas syringae. Mol. Microbiol. 45:397-409.
11. 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.
12. Brito, B., Aldon, D., Barberis, P., Boucher, C., and Genin, S. 2002. A signal transfer system through three compartments transduces the plant cell contact-dependent signal controlling Ralstonia solanacearum hrp genes. Mol. Plant-Microbe Interact. 15:109-119.
13. Bronstein, P. A., Marrichi, M., Cartinhour, S., Schneider, D. J., and DeLisa, M. P. 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.
14. Brown, D. G. and Allen, C. 2004. Ralstonia solanacearum genes induced during growth in tomato: An inside view of bacterial wilt. Mol. Microbiol. 53:1641-1660.
15. 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.
16. 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.
17. Chang, J. H., Urbach, J. M., Law, T. F., Arnold, L. W., Hu, A., Gombar, S., Grant, S. R., Ausubel, F. M., and Dangl, J. L. 2005. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl. Acad. Sci. U.S.A. 102:2549-2554.
18. Chatterjee, A., Cui, Y., and Chatterjee, A. K. 2002. Regulation of Envinia camtovora hrpL(Ecc) (sigma-L(Ecc)). which encodes an extracytoplasmic function subfamily of sigma factor required for expression of the HRP regulon. Mol. Plant-Microbe Interact. 15:971-980.
19. Chatterjec, A., Cui, Y., Liu, Y., Dumenyo, C. K., and Chatterjee. A. K. 1995. Inactivation of rsmA leads to overproduction of extracellular pectinases. ceHulases, and proteases in Erwinia camtovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl. Environ. Microbiol. 61:1959-1967.
20. Chatterjee, A., Cui, Y., Yang, H., CoHmer, A., Alfano, J. R., and Chatterjee, A. K. 2003. GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA. trascriptional activators, and alternate sigma factors. Mol. Plant-Microbe Interact. 16:1106-1117.
21. Cunnac, S., Boucher, C., and Genin, S. 2004a. Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the type III secretion system and effector genes in Ralstonia solanacearum. J. Bacteriol. 186:2309-2318.
22. Cunnac, S., Occhialini, A., Barberis, P., Boucher, C., and Genin, S. 2004b. Inventory and functional analysis of the large Hrp regulon in Ralstonia solanaceanun: Identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol. Microbiol. 53:115-128.
23. 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., Cnrsino-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., Menek, 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.
24. Dasgupta, N., Lykken, G. L., Wolfgang, M. C., and Yahr, T. L. 2004. A novel anti-anti-activator mechanism regulates expression of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 53:297-308.
25. Feil, H., Feil, W. S., Chain, P., Larimer, F. Dibartolo, G., Copeland, A., Lykidis, A., Trong, S., Nolan, M., Goltsman, E., Thiel, J., Malfatti, S., Loper, J. E., Lapidus, A., Detter, J. C., Land, M., Richardson, P. M., Kyrpides, N. C., Ivanova, N., and Lindow, S. E. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syrinxae B728a and pv. tomato DC3000. Proc. Natt. Acad. Sci. U.S.A. 102:11064-11069.
26. Fouts, D. E., Abramovitch, R. B., Alfano, J. R., Baldo, A. M., Buell, C. R., Cartinhour, S., Chatterjee, A. K., D'Ascenzo, M., Gwinn, M. L., Lazui-owitz, S. G., Lin, N. C., Martin, G. B., Rehm. A. H., Schneider, D. J., van Dijk, K., Tang, X., and Collmer A. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. U.S.A. 99:2275-2280.
27. Francis, M. S., Wolf-Watz, H., and Forsberg, A. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-172.
28. Frederick, R. D., Ahmad, M., Majerczak, D. R., Arroyo-Rodriguez, A. S., Manulis, S., and Coplin, D. L. 2001. Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. Mol. Plant-Microbe Interact. 14:1213-1222.
29. 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 11 secretory proteins in Xanthomonas oryzae pv. oryzae. J. Bacteriol. 186:1374-1380.
30. Galan, J. E., and Collmer, A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science 284:1322-1328.
31. Genin, S., Brito, B., Denny, T. P., and Boucher, C. 2005. Control of the Ralstonia solanacearum Type III secretion system (Hrp) genes by the global virulence regulator PhcA. FEBS (Fed. Eur. Biochem. Soc.) Lett. 579:2077-2081.
32. Genin, S., Gough, C. L., Zischek, C., and Boucher, C. A. 1992. Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol. Microbiol. 6:3065-3076.
33. Glickmann, E., Gardan, L., Jacquet, S., Hussain, S., Elasri, M., Petit, A., and Dessaux, Y. 1998. Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol. Plant-Microbe Interact. 11:156-162.
34. Grimm, C., Aufsatz, W., and Panopoulos, N. J. 1995. The hrpRS locus of Pseudomonas syringae pv. phaseolicola constitutes a complex regulatory unit. Mol. Microbiol. 15:155-165.
35. Heeb, S., and Haas, D. 2001. Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol. Plant-Microbe Interact. 14:1351-1363.
36. Hendrickson, E. L., Guevera, P., and Ausubel, F. M. 2000. The alternative sigma factor RpoN is required for hip activity in Pseudomonas syringae pv. maculicola and acts at the level of hrpL transcription. J. Bacteriol. 182:3508-3516.
37. Hovey, A. K., and Frank, D. W. 1995. Analysis of the DNA-binding and transcriptional activation properties of ExsA, a transcriptional activator of Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 177:4427-4436.
38. Hutcheson, S. W., Bretz, J., Sussan, T., Jin, S., and Pak, K. 2001. Enhancer-binding proteins HrpR and HrpS interact Io regulate hrp-encoded type III protein secretion in Pseudomonas syringae strains. J. Bacteriol. 183:5589-5598.
39. 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.
40. Jin, Q., und He, S.Y. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syrigae. Science 294:2556-2558.
41. Joardar, V., Lindeberg, M., Jackson, R., Selengut, J., Dodson, R., Brinkac, L. M., Daugherty, S. C., Dehoy, R., Durkin, A. S., Giglio, M. G., Madupu, R., Nelson, W. C., Rosovitz, M. J., Sullivan, S., Crabtree, J., Creasv, T., Davidsen, T., Haft, D. H., Zafar, N., Zhou, L., Halpin, R., Holley, T., Khouri, H., Feldblyum, T., While, O., Fraser, C. M., Challerjec, A. K., Cartinhour, S., Schneider, D. J., Mansfield, J., Collmer, A., and Buell, C. R. 2005. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187:6488-6498.
42. Kamdar, H. V., Kamoun, S., and Kado, C. I. 1993. Restoration of pathogenicity avirulent Xanthomonas oryzof pv. oryzae and X. camspestris pathovars by reciprocal complementation with the hrpXo and hrpXc genes and identification of HrpX function by sequence analyses. J. Bacteriol. 175:2017-2025.
43. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., Galan, J. E., and Aizawa, S. I. 1998. Supramolccular structure of the Salmonella typhimutium type III protein secretion system. Science 280:602-605.
44. Lan, L., Deng, X., Zhou, J., and Tang, X. 2006. Genome-wide gene expression analysis of Pseudomonas syringae pv. tomato DC3000 reveals overlapping and distinct pathways regulated by hrpL and hrpRS. Mol. Plant-Microbe Interact. 19:976-987.
45. Li, C. M., Brown, I., Mansfield, J., Stevens, C., Bourcau, T., Romantschuk, M., and Taira, S. 2002. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO (Eur. Mol. Biol. Organ.) J. 21:1909-1915.
46. Liu, Y., Cui, Y. Mukherjee, A., and Chatterjee, A. K. 1998. Characterization of a novel RNA regulator of Erwinio corotovora ssp. Corotovora that controls production of extracellular enzymes and secondary metabolites. Mol. Microbiol. 29:219-234.
47. Losada, L., Sussan, T. Pak, K., Zeyad, S., Rozenbaum, I., and Hutcheson. S. W. 2004. Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulencc functions by a HrpL-dependent promoter-trap assay. Mol. Plant-Microbe Interact. 17:254-262.
48. Losada, L. C. and Hutcheson, S. W. 2005. Type III secretion chaperones of Pseudomonas syringae protect effectors from Lon-associated degradation. Mol. Microbiol. 55:941-953.
49. Marenda, M., Brito, B., Callard, D., Genin, S., Barberis, P., Boucher, C., and Arlat, M. 1998. PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells. Mol. Microbioi. 27:437-453.
50. Marlovits, T. C., Kubori, T., Sukhan, A., Thomas, D. R., Galan, J. E., and Unger, V. M. 2004. Structural insights into the assembly of the type III secretion needle complex. Science 306:1040-1042.
51. McCaw, M. L., Lykken, G. L., Singh, P. K., and Yahr, T. L. 2002. ExsD is a negative regulator of the Pseudomonas aeruginosa type III secretion regulon. Mol. Microbiol. 46:1123-1133.
52. Merighi, M., Majerczak, D. R., Stover, E. H., and Coplin, D. L. 2003. The HrpX/HrpY two-component system activates hrpS expression, the first step in the regulatory cascude controlling the Hrp regulon in Pantoea stewartii subsp. stewartii Mol. Plant-Microbe Interact. 16:238-248.
53. Mittal, S., and Davis, K. R. 1995. Role of the phytotoxin coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 8:165-171.
54. Mor, H., Manulis, S., Zuck, M., Nizan, R., Coplin, D. L., and Barash, I. 2001. Genetic organization of the hrp gene cluster and dspAE/BF operon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 14:431-436.
55. Mukaihara, T., Tumura, N., Murata, Y., and Iwubuchi, M. 2004. Genetic screening of Hrp type III-related pathogenicity genes controlled by the HrpB transcriptional activator in Ralstonia solanaccarum. Mol. Microbiol. Mol. Microbiol. 54:863-875.
56. Nissan, G., Manulis, S., Weinthal, D. M., Sessa, G., and Barash, I. 2005. Analysis of promoters recognized by HrpL, an alternative sigma-factor protein from Pantoea agglomerans pv. gvpsophilae. Mol. Plant-Microbe Interact. 18:634-643.
57. Nizan-Koren, R., Manulis, S., Mor, H., Iraki, N. M., and Barash, I. 2003. The regulatory cascade that activates the Hrp regulon in Erwinia herbicola pv. gypsophilae. Mol. Plant-Microbe Interact. 16:249-260.
58. Noel, L., Thieme, F., Nennstiel, D., and Bonas, U. 2001. cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campertris pv. vesicatoria. Mol. Microbiol. 41:1271-1281.
59. Occhialini, A., Cunnac, S., Reymond, N., Genin, S., and Boucher, C. 2005. Genome-wide analysis of gene expression in Ralstonia solanacearum reveals that the hrpB gene acts as a regulatory switch controlling multiple virulence pathways. Mol. Plant-Microbe Interact. 18:938-949.
60. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K. E., and Wolf-Watz. H. 1996. Modulation of virulence factor expression by pathogen target cell conlact. Science 273:1231-1233.
61. Preston, G., Deng, W. L., Huang, H. C., and Collmer, A. 1998. Negative regulation of hrp genes in Pseudomonas syringae by HrpV. J. Bacteriol. 180:4532-4537.
62. Rahme, L. G., Mindrinos, M. N., and Panopoulos, N. J. 1992. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J. Bacteriol. 174:3499-3507.
63. Roine, E., Wei, W., Yuan, J., Nurmialio-Lassila, E. L., Kalkkinen, N., Romantschuk, M., and He, S. Y. 1997. Hrp pilus: An hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 94:3459-3464.
64. Schell, M. A. 2000. Control of virulence and pathogenicity genes of Ralstonia solanacearum by elaborate sensory network. Annu. Rev. Phytopathol. 38:263-292.
65. Schulte, R., and Bonus, U. 1992. Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hyperscnsitivity on pepper and tomato, is plant inducible. J. Bacteriol. 174:815-823.
66. Stainier, I., Iriarte, M., and Cornelis, G. R. 1997. YscMI and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription. Mol. Microbiol. 26:833-843.
67. Thieme, F., Kocbnik, R., Bekel, T., Berger, C., Boch, J., Buttner, D., Caldana, C., Gaigalat, L., Goesmann, A., Kay, S., Kirchner, O., Lanz., C., Linke, B., McHardy, A. C., Meyer, F., Mittenhuber, G., Nies, D. H., Niesbach-Klosgen, U., Patschkowski, T., Rucken, C., Rupp, O., Schneiker, S., Schuster, S. C., Vorholten F. J., Weber, E., Puhler. A., Bonas, U., Bartels, D., and Kaiser. O. 2005. Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J. Bactcriol. 187:7254-7266.
68. Thwaites, R., Spanu, P. D., Panopoulos, N. J., Stevens, C., and Mansfield. J. W., 2004. Transcriptional regulation of components of the type III secretion system and effectors in Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact. 17:1250-1258.
69. Tsuge, S., Terashima, S., Furutani, A., Ochiai, H., Oku, T., Tsuno, K., Kaku, H., and Kubo, Y. 2005. Effects on promoter activity of base substitutions in the cis-acting regulatory element of HrpXo regulons in Xanthomonas oryzae pv. orvzae. J. Bacteriol. 187:2308-2314.
70. van Dijk, K., Fonts, D. E., Rehm, A. H., Hill, A. R., Collmer, A., and Alfano, J. R. 1999. The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseadomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J. Bacteriol. 181:4790-4797.
71. 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.
72. Weber, E., Ojanen-Reuhs, T., Huguet, E., Hause, G., Romantschuk, M., Korhonen, T. K., Bonas, U., and Koebnik, R. 2005. The type III-dependent Hrp pilus is required tor productive inieraction of Xanthomonas campestris pv. vesicatoria with pepper host plants. J. Bacteriol. 187:2458-2468.
73. Wei, C. F., Deng, W. L., and Huang, H. C., 2005. A chaperone-like HrpG protein acts as a suppressor of HrpV in regulation of the Pseudomonas syringae pv. syringae type III secretion system. Mol. Microbiol. 57:520-536.
74. Wei, W., Plovanich-Jones, A., Deng, W. L., Jin, Q. L., Collmer, A., Huang, H. C., and He, S. Y., 2000a. The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas svingae pv. tomato. Proc. Natl. Acad. Sci. U.S.A. 97:2247-2252.
75. Wei, Z., Kim, J. F. and Beer. S. V. 2000b. Regulation of hrp genes and type III protein secretion in Erwinia amylovora by HrpX/HrpY, a novel two-component system, and HrpS. Mol. Plant-Microbe Interact. 13:1251-1262.
76. Wei, Z. M., and Beer, S. V. 1995. hrpL activates Envinia amylovora hrp gene transcription and is a member of the FCF subfamily of sigma factors. J. Bacteriol. 177:6201-6210.
77. Wei, Z. M., Sneath, B. J., and Beer, S. V. 1992. Expression of Erwinia amylovora hrp genes in response to environmental stimuli. J. Bacteriol. 174:1875-1882.
78. Wengelnik, K., and Bonas, U. 1996. HrpXv. an AraC-type regulator, activates expression of five of the six loci in the hip cluster of Xamhomonas campestris pv. vesicatoria. J. Bacteriol. 178:3462-3469.
79. Wengelnik, K., Rossier, O., and Bonas, U. 1999. Mutations in the regulatory gene hrpC of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. J. Bacteriol. 181:6828-6831.
80. Wengelnik, K., Van den Ackerveken, G., and Bonas, U. 1996. HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol. Plant-Microbe Interact. 9:704-712.
81. Xiao, F., Goodwin, S. M., Xiao, Y., Sun, Z., Baker, D., Tang, X., Jenks, M. A., and Zhou, J. M., 2004. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO (Eur. Mol. Biol. Organ.) J. 23:2903-2913.
82. Xiao, Y., Heu, S., Yi, J., Lu, Y., and Hutcheson, S. W. 1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J. Bacteriol. 176:1025-1036.
83. Xiao, Y., Lu, Y., Heu, S., and Hutcheson, S. W. 1992, Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J. Bacteriol. 174:1734-1741.
84. Yang, S., Perna, N. T., Cooksey, D. A., Okinaka, Y., Lindow, S. E., Ibekwe, A. M., Keen, N. T., and Yang, C. H. 2004. Genome-wide identification of plant-upregulated genes of Erwinia chrysanthemi 3937 using a GFP-based IVET leaf array. Mol. Plant-Microbe Interact. 17:999-1008.
85. Zwiesler-Vollick, J., Plovanich-Jones, A. E., Nomura, K., Bandyopadhyay, S., Joardar, V., Kunkel, B. N., and He, S. Y. 2002. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45:1207-1218.