The noncanonical type III secretion system of Xanthomonas translucens pv. graminis is essential for forage grass infection

Molecular Plant Pathology

Volumn 14, Issue 6, 2013, Pages 576-588

  Wichmann, Fabienne ^a,c   Vorhölter, Frank Jörg ^b   Hersemann, Lena ^a   Widmer, Franco ^a   Blom, Jochen ^b   Niehaus, Karsten ^b   Reinhard, Sonja ^a   Conradin, Constanze ^a   Kölliker, Roland ^a  

^a AGROSCOPE RECKENHOLZ TÄNIKON RESEARCH STATION ART   (Switzerland)

^b BIELEFELD UNIVERSITY   (Germany)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; POACEAE; XANTHOMONAS;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; POACEAE; XANTHOMONAS;

EID: 84879861793     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12030     Document Type: Article

References (90)

1. Alegria, M.C., Souza, D.P., Andrade, M.O., Docena, C., Khater, L., Ramos, C.H.I., da Silva, A.C.R. and Farah, C.S. (2005) Identification of new protein-protein interactions involving the products of the chromosome- and plasmid-encoded type IV secretion loci of the phytopathogen Xanthomonas axonopodis pv. citri. J. Bacteriol. 187, 2315-2325.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
3. 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.
4. Ausubel, F., Brent, R., Kinston, R., Moore, D., Seidman, J., Smith, J. and Struhl, K. (1987) Current Protocols in Molecular Biology. New York: J. Wiley & Sons.
5. Becker, A., Katzen, F., Pühler, A. and Ielpi, L. (1998) Xanthan gum biosynthesis and application: a biochemical/genetic perspective. Appl. Microbiol. Biotechnol. 50, 145-152.
6. Blom, J., Albaum, S.P., Doppmeier, D., Pühler, A., Vorhölter, F.J., Zakrzewski, M. and Goesmann, A. (2009) EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics, 10, 14.
7. Bogdanove, A.J., Koebnik, R., Lu, H., Furutani, A., Angiuoli, S.V., Patil, P.B., Van Sluys, M.-A., Ryan, R.P., Meyer, D.F., Han, S.-W., Aparna, G., Rajaram, M., Delcher, A.L., Phillippy, A.M., Puiu, D., Schatz, M.C., Shumway, M., Sommer, D.D., Trapnell, C., Benahmed, F., Dimitrov, G., Madupu, R., Radune, D., Sullivan, S., Jha, G., Ishihara, H., Lee, S.-W., Pandey, A., Sharma, V., Sriariyanun, M., Szurek, B., Vera-Cruz, C.M., Dorman, K.S., Ronald, P.C., Verdier, V., Dow, J.M., Sonti, R.V., Tsuge, S., Brendel, V.P., Rabinowicz, P.D., Leach, J.E., White, F.F. and Salzberg, S.L. (2011) Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J. Bacteriol. 193, 5450-5464.
8. Brummer, E.C. (1999) Capturing heterosis in forage crop cultivar development. Crop Sci. 39, 943-954.
9. Büttner, D. and Bonas, U. (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol. Rev. 34, 107-133.
10. Büttner, D. and He, S.Y. (2009) Type III protein secretion in plant pathogenic bacteria. Plant Physiol. 150, 1656-1664.
11. Büttner, D., Nennstiel, D., Klusener, B. and Bonas, U. (2002) Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 184, 2389-2398.
12. Büttner, D., Noël, L., Stuttmann, J. and Bonas, U. (2007) Characterization of the nonconserved hpaB-hrpF region in the hrp pathogenicity island from Xanthomonas campestris pv. vesicatoria. Mol. Plant-Microbe Interact. 20, 1063-1074.
13. Cho, H.J., Park, Y.J., Noh, T.H., Kim, Y.T., Kim, J.G., Song, E.S., Lee, D.H. and Lee, B.M. (2008) Molecular analysis of the hrp gene cluster in Xanthomonas oryzae pathovar oryzae KACC10859. Microb. Pathog. 44, 473-483.
14. Da Silva, A.C.R., 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.C., Do Amaral, A.M., Bertolini, M.C., Camargo, L.E.A., Camarotte, G., Cannavan, F., Cardozo, J., Chambergo, F., Clapina, L.P., Cicarelli, R.M.B., Coutinho, L.L., Cursino-Santos, J.R., El-Dorry, H., Faria, J.B., Ferreira, A.J.S., Ferreira, R.C.C., Ferro, M.I.T., Formighieri, E.F., Franco, M.C., Greggio, C.C., Gruber, A., Katsuyama, A.M., Kishi, L.T., Leite, R.P., Lemos, E.G.M., Lemos, M.V.F., Locali, E.C., Machado, M.A., Madeira, A., Martinez-Rossi, N.M., Martins, E.C., Meidanis, J., Menck, C.F.M., Miyaki, C.Y., Moon, D.H., Moreira, L.M., Novo, M.T.M., Okura, V.K., Oliveira, M.C., Oliveira, V.R., Pereira, H.A., Rossi, A., Sena, J.A.D., Silva, C., De Souza, R.F., Spinola, L.A.F., Takita, M.A., Tamura, R.E., Teixeira, E.C., Tezza, R.I.D., Dos Santos, M.T., 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.
15. Darsonval, A., Darrasse, A., Meyer, D., Demarty, M., Durand, K., Bureau, C., Manceau, C. and Jacques, M.A. (2008) The type III secretion system of Xanthomonas fuscans subsp fuscans is involved in the phyllosphere colonization process and in transmission to seeds of susceptible beans. Appl. Environ. Microbiol. 74, 2669-2678.
16. Delcher, A.L., Bratke, K.A., Powers, E.C. and Salzberg, S.L. (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics, 23, 673-679.
17. Dobrindt, U., Hochhut, B., Hentschel, U. and Hacker, J. (2004) Genomic islands in pathogenic and environmental microorganisms. Nat. Rev. Microbiol. 2, 414-424.
18. Egli, T. and Schmidt, D. (1982) Pathogenic variation among the causal agents of bacterial wilt of forage grasses. J. Phytopathol. 104, 138-150.
19. Egli, T., Goto, M. and Schmidt, D. (1975) Bacterial wilt, a new forage grass disease. J. Phytopathol. 82, 111-121.
20. 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 systems. Mol. Plant-Microbe Interact. 8, 845-854.
21. Furutani, A., Takaoka, M., Sanada, H., Noguchi, Y., Oku, T., Tsuno, K., Ochiai, H. and Tsuge, S. (2009) Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 22, 96-106.
22. Gophna, U., Ron, E.Z. and Graur, D. (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene, 312, 151-163.
23. Gurlebeck, D., Thieme, F. and Bonas, U. (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. J. Plant Physiol. 163, 233-255.
24. Hajri, A., Brin, C., Hunault, G., Lardeux, F., Lemaire, C., Manceau, C., Boureau, T. and Poussier, S. (2009) A 'repertoire for repertoire' hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLoS ONE, 4, 21.
25. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
26. Hauben, L., Vauterin, L., Swings, J. and Moore, E.R.B. (1997) Comparison of 16S ribosomal DNA sequences of all Xanthomonas species. Int. J. Syst. Bacteriol. 47, 328-335.
27. Horton, R.M. (1995) PCR-mediated recombination and mutagenesis. Mol. Biotechnol. 3, 93-99.
28. Hothorn, T., Hornik, K., Van de Wiel, M.A. and Zeileis, A. (2006) A lego system for conditional inference. Am. Stat. 60, 257-263.
29. Hyatt, D., Chen, G.-L., LoCascio, P.F., Land, M.L., Larimer, F.W. and Hauser, L.J. (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics, 11, 119.
30. Jiang, B., Xu, R.Q., Li, X.Z., Wei, H.Y., Bai, F., Hu, X., He, Y.Q. and Tang, J.L. (2006) Construction and characterization of a hrpG mutant rendering constitutive expression of hrp genes in Xanthomonas campestris pv. campestris. Prog. Nat. Sci. 16, 480-485.
31. Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
32. Kaniga, K., Delor, I. and Cornelis, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria-inactivation of the blaA gene of Yersinia enterocolitica. Gene, 109, 137-141.
33. Kay, S. and Bonas, U. (2009) How Xanthomonas type III effectors manipulate the host plant. Curr. Opin. Microbiol. 12, 37-43.
34. Kieleczawa, J. (2006) Fundamentals of sequencing of difficult templates-an overview. J. Biomol. Tech., 17, 207-217.
35. Kim, J.G., Li, X.Y., Roden, J.A., Taylor, K.W., Aakre, C.D., Su, B., Lalonde, S., Kirik, A., Chen, Y.H., Baranage, G., McLane, H., Martin, G.B. and Mudgett, M.B. (2009) Xanthomonas T3S effector XopN suppresses PAMP-triggered immunity and interacts with a tomato atypical receptor-like kinase and TFT1. Plant Cell, 21, 1305-1323.
36. Kölliker, R., Kraehenbuehl, R., Boller, B. and Widmer, F. (2006) Genetic diversity and pathogenicity of the grass pathogen Xanthomonas translucens pv. graminis. Syst. Appl. Microbiol. 29, 109-119.
37. Krause, L., McHardy, A.C., Nattkemper, T.W., Pühler, A., Stoye, J. and Meyer, F. (2007) GISMO-gene identification using a support vector machine for ORF classification. Nucleic Acids Res. 35, 540-549.
38. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. and Higgins, D.G. (2007) ClustalW and ClustalX version 2. Bioinformatics, 23, 2947-2948.
39. 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., 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.
40. Leyns, F. (1993) Xanthomonas campestris pv. graminis: cause of bacterial wilt of forage grasses. In: Xanthomonas (Swings, J.G. and Civerolo, E.L., eds), pp. 55-57. London: Chapman & Hall.
41. Linke, B., McHardy, A.C., Neuweger, H., Krause, L. and Meyer, F. (2006) REGANOR: a gene prediction server for prokaryotic genomes and a database of high quality gene predictions for prokaryotes. Appl. Bioinformatics, 5, 193-198.
42. Masuch, G., Schoene, K. and Paul, V.H. (1989) Histological investigations on the pathogenesis of Xanthomonas campestris pv. graminis to Lolium multiflorum. EPPO Bull. 19, 73-80.
43. Metz, M., Dahlbeck, D., Morales, C.Q., Al Sady, B., Clark, E.T. and Staskawicz, B.J. (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J. 41, 801-814.
44. Meyer, F., Goesmann, A., McHardy, A.C., Bartels, D., Bekel, T., Clausen, J., Kalinowski, J., Linke, B., Rupp, O., Giegerich, R. and Pühler, A. (2003) GenDB-an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 31, 2187-2195.
45. Michel, V.V. (2001) Interactions between Xanthomonas campestris pv. graminis strains and meadow fescue and Italian rye grass cultivars. Plant Dis. 85, 538-542.
46. Moreira, L.M., De Souza, R.F., Digiampietri, L.A., Da Silva, A.C.R. and Setubal, J.C. (2005) Comparative analyses of Xanthomonas and Xylella complete genomes. Omics, 9, 43-76.
47. Moreira, L.M., Almeida, N.F., Potnis, N., Digiampietri, L.A., Adi, S.S., Bortolossi, J.C., da Silva, A.C., da Silva, A.M., de Moraes, F.E., de Oliveira, J.C., de Souza, R.F., Facincani, A.P., Ferraz, A.L., Ferro, M.I., Furlan, L.R., Gimenez, D.F., Jones, J.B., Kitajima, E.W., Laia, M.L., Leite, R.P., Nishiyama, M.Y., Neto, J.R., Nociti, L.A., Norman, D.J., Ostroski, E.H., Pereira, H.A., Staskawicz, B.J., Tezza, R.I., Ferro, J.A., Vinatzer, B.A. and Setubal, J.C. (2010) Novel insights into the genomic basis of citrus canker based on the genome sequences of two strains of Xanthomonas fuscans subsp. aurantifolii. BMC Genomics, 11, 238.
48. Moscou, M.J. and Bogdanove, A.J. (2009) A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501.
49. Mudgett, M.B., Chesnokova, O., Dahlbeck, D., Clark, E.T., Rossier, O., Bonas, U. and Staskawicz, B.J. (2000) Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. USA, 97, 13324-13329.
50. Mukherjee, S., Hao, Y.H. and Orth, K. (2007) A newly discovered post-translational modification-the acetylation of serine and threonine residues. Trends Biochem. Sci. 32, 210-216.
51. Noël, L., Thieme, F., Nennstiel, D. and Bonas, U. (2001) cDNA analysis unravels a genome-wide HrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol. Microbiol. 41, 1271-1281.
52. Noël, L., Thieme, F., Nennstiel, D. and Bonas, U. (2002) Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J. Bacteriol. 184, 1340-1348.
53. Noël, L., Thieme, F., Gabler, J., Büttner, D. and Bonas, U. (2003) XopC and XopJ, two novel type III effector proteins from Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 185, 7092-7102.
54. Ochiai, H., Inoue, V., Takeya, M., Sasaki, A. and Kaku, H. (2005) Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Japan Agric. Research Quart. 39, 275-287.
55. Oshiro, E.E., Nepomuceno, R.S.L., Faria, J.B., Ferreira, L.C.S. and Ferreira, R.C.C. (2006) Site-directed gene replacement of the phytopathogen Xanthomonas axonopodis pv. citri. J. Microbiol. Methods, 65, 171-179.
56. Parkinson, N., Cowie, C., Heeney, J. and Stead, D. (2009) Phylogenetic structure of Xanthomonas determined by comparison of gyrB sequences. Int. J. Syst. Evol. Microbiol. 59, 264-274.
57. Patil, P.B., Bogdanove, A.J. and Sonti, R.V. (2007) The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice, citrus and crucifers. BMC Evol. Biol. 7, 243.
58. Pieretti, I., Royer, M., Barbe, V., Carrere, S., Koebnik, R., Cociancich, S., Couloux, A., Darrasse, A., Gouzy, J., Jacques, M.A., Lauber, E., Manceau, C., Mangenot, S., Poussier, S., Segurens, B., Szurek, B., Verdier, V., Arlat, M. and Rott, P. (2009) The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics, 10, 15.
59. Qian, W., Jia, Y.T., Ren, S.X., He, Y.Q., Feng, J.X., Lu, L.F., Sun, Q.H., Ying, G., Tang, D.J., Tang, H., Wu, W., Hao, P., Wang, L.F., Jiang, B.L., Zeng, S.Y., Gu, W.Y., Lu, G., Rong, L., Tian, Y.C., Yao, Z.J., Fu, G., Chen, B.S., Fang, R.X., Qiang, B.Q., Chen, Z., Zhao, G.P., Tang, J.L. and He, C.Z. (2005) Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Resi. 15, 757-767.
60. Roden, J.A., Belt, B., Ross, J.B., Tachibana, T., Vargas, J. and Mudgett, M.B. (2004) A genetic screen to isolate type III effectors translocated into pepper cells during Xanthomonas infection. Proc. Natl. Acad. Sci. USA, 101, 16624-16629.
61. Römer, P., Recht, S. and Lahaye, T. (2009a) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc. Natl. Acad. Sci. USA, 106, 20526-20531.
62. Römer, P., Strauss, T., Hahn, S., Scholze, H., Morbitzer, R., Grau, J., Bonas, U. and Lahaye, T. (2009b) Recognition of AvrBs3-like proteins is mediated by specific binding to promoters of matching pepper Bs3 Alleles. Plant Physiol. 150, 1697-1712.
63. Rossier, O., Van den Ackerveken, G. and Bonas, U. (2000) HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol. Microbiol. 38, 828-838.
64. Ryan, R.P. and Dow, J.M. (2011) Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. Trends Microbioli. 19, 145-152.
65. Ryan, R.P., Vorhölter, F.-J., Potnis, N., Jones, J.B., Van Sluys, M.-A., Bogdanove, A.J. and Dow, J.M. (2011) Pathogenomics of Xanthomonas: understanding bacterium × plant interactions. Nat. Rev. Microbiol. 9, 344-355.
66. 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., Wincker, P., Levy, M., Weissenbach, J. and Boucher, C. (2002) Genome sequence of the plant pathogen Ralstonia solanacearum. Nature, 415, 497-502.
67. Salzberg, S.L., Sommer, D.D., Schatz, M.C., Phillippy, A.M., Rabinowicz, P.D., Tsuge, S., Furutani, A., Ochiai, H., Delcher, A.L., Kelley, D., Madupu, R., Puiu, D., Radune, D., Shumway, M., Trapnell, C., Aparna, G., Jha, G., Pandey, A., Patil, P.B., Ishihara, H., Meyer, D.F., Szurek, B., Verdier, V., Koebnik, R., Dow, J.M., Ryan, R.P., Hirata, H., Tsuyumu, S., Lee, S.W., Ronald, P.C., Sonti, R.V., Van Sluys, M.A., Leach, J.E., White, F.F. and Bogdanove, A.J. (2008) Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99(A). BMC Genomics, 9, 16.
68. Schatschneider, S., Vorhölter, F.-J., Rueckert, C., Becker, A., Eisenreich, W., Pühler, A. and Niehaus, K. (2011) Genome-enabled determination of amino acid biosynthesis in Xanthomonas campestris pv. campestris and identification of biosynthetic pathways for alanine, glycine, and isoleucine by (13)C-isotopologue profiling. Mol. Genet. Genomics, 286, 247-259.
69. Schwientek, P., Szczepanowski, R., Ruckert, C., Kalinowski, J., Klein, A., Selber, K., Wehmeier, U.F., Stoye, J. and Pühler, A. (2012) The complete genome sequence of the acarbose producer Actinoplanes sp SE50/110. BMC Genomics, 13, 112.
70. Song, C. and Yang, B. (2010) Mutagenesis of 18 type III effectors reveals virulence function of XopZ(PXO99) in Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 23, 893-902.
71. Studholme, D.J., Kemen, E., MacLean, D., Schornack, S., Aritua, V., Thwaites, R., Grant, M., Smith, J. and Jones, J.D.G. (2010) Genome-wide sequencing data reveals virulence factors implicated in banana Xanthomonas wilt. FEMS Microbiol. Lett. 310, 182-192.
72. Studholme, D.J., Wasukira, A., Paszkiewicz, K., Aritua, V., Thwaites, R., Smith, J. and Grant, M. (2011) Draft genome sequences of Xanthomonas sacchari and two banana-associated xanthomonads reveal insights into the Xanthomonas Group 1 Clade. Gene, 2, 1050-1065.
73. Sugio, A., Yang, B. and White, F.F. (2005) Characterization of the hrpF pathogenicity peninsula of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 18, 546-554.
74. Sun, W.X., Liu, L.J. and Bent, A.F. (2011) Type III secretion-dependent host defence elicitation and type III secretion-independent growth within leaves by Xanthomonas campestris pv. campestris. Mol. Plant Pathol. 12, 731-745.
75. Swords, K.M.M., Dahlbeck, D., Kearney, B., Roy, M. and Staskawicz, B.J. (1996) Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J. Bacteriol. 178, 4661-4669.
76. The R Development Core Team (2008) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
77. Thieme, F., Koebnik, R., Bekel, T., Berger, C., Boch, J., Büttner, 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., Ruckert, C., Rupp, O., Schneiker, S., Schuster, S.C., Vorhölter, F.-J., Weber, E., Pühler, 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. Bacteriol. 187, 7254-7266.
78. Thieme, F., Szczesny, R., Urban, A., Kirchner, O., Hause, G. and Bonas, U. (2007) New type III effectors from Xanthomonas campestris pv. vesicatoria trigger plant reactions dependent on a conserved N-myristoylation motif. Mol. Plant-Microbe Interact. 20, 1250-1261.
79. Van Sluys, M.A., Monteiro-Vitorello, C.B., Camargo, L.E.A., Menck, C.F.M., da Silva, A.C.R., Ferro, J.A., Oliveira, M.C., Setubal, J.C., Kitajima, J.P. and Simpson, A.J. (2002) Comparative genomic analysis of plant-associated bacteria. Annu. Rev. Phytopathol. 40, 169-189.
80. Vorhölter, F.J., Thias, T., Meyer, F., Bekel, T., Kaiser, O., Pühler, A. and Niehaus, K. (2003) Comparison of two Xanthomonas campestris pathovar campestris genomes revealed differences in their gene composition. J. Biotechnol. 106, 193-202.
81. Vorhölter, F.J., Schneiker, S., Goesmann, A., Krause, L., Bekel, T., Kaiser, O., Linke, B., Patschkowski, T., Rueckert, C., Schmid, J., Sidhu, V.K., Sieber, V., Tauch, A., Watt, S.A., Weisshaar, B., Becker, A., Niehaus, K. and Puehler, A. (2008) The genome of Xanthomonas campestris pv. campestris B 100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis. J. Biotechnol. 134, 33-45.
82. Wang, K., Kang, L., Anand, A., Lazarovits, G. and Mysore, K.S. (2007) Monitoring inplanta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv. New Phytol. 174, 212-223.
83. Wei, C.F., Kvitko, B.H., Shimizu, R., Crabill, E., Alfano, J.R., Lin, N.C., Martin, G.B., Huang, H.C. and Collmer, A. (2007) A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 51, 32-46.
84. Wengelnik, K., VandenAckerveken, 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.
85. Wengelnik, K., Rossier, O. and Bonas, U. (1999) Mutations in the regulatory gene hrpG of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. J. Bacteriol. 181, 6828-6831.
86. Whalen, M.C., Wang, J.F., Carland, F.M., Heiskell, M.E., Dahlbeck, D., Minsavage, G.V., Jones, J.B., Scott, J.W., Stall, R.E. and Staskawicz, B.J. (1993) Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii-7998. Mol. Plant-Microbe Interact. 6, 616-627.
87. White, F., Potnis, N., Jones, J. and Koebnik, R. (2009) The type III effectors of Xanthomonas. Mol. Plant Pathol. 10, 749-766.
88. Wichmann, F., Hug, B.M., Widmer, F., Boller, B., Studer, B. and Kölliker, R. (2011) Phenotypic and molecular genetic characterization indicate no major race-specific interactions between Xanthomonas translucens pv. graminis and Lolium multiflorum. Plant Pathol. 60, 314-324.
89. Yoshimochi, T., Zhang, Y., Kiba, A., Hikichi, Y. and Ohnishi, K. (2009) Expression of hrpG and activation of response regulator HrpG are controlled by distinct signal cascades in Ralstonia solanacearum. J. Gen. Plant Pathol. 75, 196-204.
90. Zou, L.F., Wang, X.P., Xiang, Y., Zhang, B., Li, Y.R., Xiao, Y.L., Wang, J.S., Walmsley, A.R. and Chen, G.Y. (2006) Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Appl. Environ. Microbiol. 72, 6212-6224.