A multilocus sequence analysis of Xanthomonas campestris reveals a complex structure within crucifer-attacking pathovars of this species

Systematic and Applied Microbiology

Volumn 34, Issue 2, 2011, Pages 156-165

  Fargier, E ^a,b   Saux, M Fischer Le ^a   Manceau, C ^a  

^a CEMAGREF   (France)

^b GEVES SNES   (France)

Author keywords

Brassicaceae; Cruciferae; Cruciferous plants; Multilocus sequence analysis; Pathovar; Plant pathogen; Recombination; Taxonomy; Xanthomonas

Indexed keywords

BACTERIAL DNA;

ARTICLE; DNA SEQUENCE; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC VARIABILITY; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; XANTHOMONAS ABERRANS; XANTHOMONAS ARMORACIAE; XANTHOMONAS BARBAREAE; XANTHOMONAS CAMPESTRIS; XANTHOMONAS INCANAE; XANTHOMONAS RAPHANI;

BACTERIAL TYPING TECHNIQUES; BRASSICACEAE; GENETIC LINKAGE; GENETIC VARIATION; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; RECOMBINATION, GENETIC; XANTHOMONAS CAMPESTRIS;

BACTERIA (MICROORGANISMS); BRASSICACEAE; XANTHOMONAS; XANTHOMONAS CAMPESTRIS;

EID: 79952538532     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2010.09.001     Document Type: Article

References (61)

1. Ah-You N., Gagnevin L., Grimont P.A.D., Brisse S., Nesme X., Chiroleu F., Bui Thi Ngoc L., Jouen E., Lefeuvre P., Verniere C., Pruvost O. Polyphasic characterization of xanthomonads pathogenic to members of the Anacardiaceae and their relatedness to species of Xanthomonas. Int. J. Syst. Evol. Microbiol. 2009, 59:306-318.
2. Alvarez A.M., Benedict A.A., Mizumoto C.Y., Hunter J.E., Gabriel D.W. Serological, pathological, and genetic diversity among strains of Xanthomonas campestris infecting crucifers. Phytopathology 1994, 84:1449-1457.
3. Bui Thi Ngoc L., Verniere C., Jouen E., Ah-You N., Lefeuvre P., Chiroleu F., Gagnevin L., Pruvost O. Amplified fragment length polymorphism and multilocus sequence analysis-based genotypic relatedness among pathogenic variants of Xanthomonas citri pv. citri and Xanthomonas campestris pv. bilvae. Int. J. Syst. Evol. Microbiol. 2010, 60:515-525.
4. Boudon S., Manceau C., Nottéghem J.L. Structure and Origin of Xanthomonas arboricola pv. pruni populations causing bacterial spot of stone fruit trees in Western Europe. Phytopathology 2005, 95:1081-1088.
5. Boureau T., Jacques M.A., Berruyer R., Dessaux Y., Dominguez H., Morris C.E. Comparison of the phenotypes and genotypes of biofilm and solitary epiphytic bacterial populations on broad-leaved endive. Microb. Ecol. 2004, 47:87-95.
6. Bradbury J.F Guide to Plant Pathogenic Bacteria 1986, CAB International Mycological Institute, Kew, Surrey, UK, pp. 198-260.
7. Castillo J.A., Greenberg J.T. Evolutionary dynamics of Ralstonia solanacearum. Appl. Environ. Microbiol. 2007, 73:1225-1238.
8. Cook A.A., Larson R.H., Walker J.C. Relation of the black rot pathogen to cabbage seed. Phytopathology 1952, 42:316-320.
9. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988, 16:10881-10890.
10. Cohan F.M. Bacterial species and speciation. Syst. Biol. 2001, 50:513-524.
11. 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., Ciapina 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.M.B.N., 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., Trindade dos Santos M., Truffi D., Tsai S.M., White F.F., Setubal J.C., Kitajima J.P. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 2002, 417:459-462.
12. Dye D.W., Bradbury J.F., Goto M., Hayward A., Lelliott R.A., Schroth M.N. International standards for naming pathovars of phytopathogenic bacteria and list of pathovar names and pathotype strains. Rev. Plant Pathol. 1980, 59:153-168.
13. Enersen M., Olsen I., van Winkelhoff A.J., Caugant D.A. Multilocus sequence typing of Porphyromonas gingivalis strains from different geographic origins. J. Clin. Microbiol. 2006, 44:35-41.
14. Fargier E., Manceau C. Pathogenicity assays restrict the Xanthomonas campestris species (Vauterin et al. 1995) into three pathovars and reveal nine races within X. campestris pv. campestris. Plant Pathol. 2007, 56:805-818.
15. Feil E.J., Holmes E.C., Bessen D.E., Chan M.S., Day N.P.J., Enright M.C., Goldstein R., Hood D.W., Kalia A., Moore C.E., Zhou J., Spratt B.G. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc. Natl. Acad. Sci. USA 2001, 98:182-187.
16. Feil E.J., Maiden M.C.J., Achtman M., Spratt B.G. The relative contributions of recombination and mutation to the divergence of clones of Neisseria meningitidis. Mol. Biol. Evol. 1999, 16:1496-1502.
17. Felsenstein J. PHYLIP (Phylogeny Inference Package) Version 3.63. 2005, Department of Genetics, University of Washington, Seattle.
18. Gevers D., Cohan F.M., Lawrence J.G., Spratt B.G., Coenye T., Feil E.J., Stackebrandt E., Van de Peer Y., Vandamme P., Thompson F.L., Swings J. Opinion: Re-evaluating prokaryotic species. Nat. Rev. Microbiol. 2005, 3:733-739.
19. Guindon S., Lethiec F., Duroux P., Gascuel O. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 2005, 33:W557-9. (Web Server issue).
20. Huson D.H., Bryant D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 2006, 23:254-267.
21. Jacques M.A., Josi K., Darrasse A., Samson R. Xanthomonas axonopodis pv. phaseoli var. fuscans is aggregated in stable biofilm population sizes in the phyllosphere of field-grown beans. Appl. Environ. Microbiol. 2005, 71:2008-2015.
22. Jolley K.A., Feil E.J., Chan M.S., Maiden M.C. Sequence type analysis and recombinational tests (START). Bioinformatics 2001, 17:1230-1231.
23. Kamdar H.V., Kamoun S., Kado C.I. Restoration of pathogenicity of avirulent Xanthomonas oryzae pv. oryzae and X. campestris pathovars by reciprocal complementation with the hrpXo and hrpXc genes and identification of HrpX function by sequence analyses. J. Bacteriol. 1993, 175:2017-2025.
24. Kendrick J.B., Baker K.F. Bacterial blight of garden stocks and its control by hot-water seed treatment. Calif. Agric. Exp. Stn. Bull. Bull. 1942, 665:1-23.
25. Koehler A., Karch H., Beikler T., Flemmig T.F., Suerbaum S., Schmidt H. Multilocus sequence analysis of Porphyromonas gingivalis indicates frequent recombination. Microbiology 2003, 149:2407-2415.
26. Kotetishvili M., Stine O.C., Kreger A., Morris J.G., Sulakvelidze A. Multilocus sequence typing for characterization of clinical and environmental Salmonella strains. J. Clin. Microbiol. 2002, 40:1626-1635.
27. 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., Go S.J. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 2005, 33:577-586.
28. Lima W.C., Paquola A.C.M., Varani A.M., Van Sluys M.-A., Menck C.F.M. Laterally transferred genomic islands in Xanthomonadales related to pathogenicity and primary metabolism. FEMS Microbiol. Lett. 2008, 281:87-97.
29. Lin N.T., Liu T.J., Lee T.C., You B.Y., Yang M.H., Wen F.S., Tseng Y.H. The adsorption protein genes of Xanthomonas campestris filamentous phages determining host specificity. J. Bacteriol. 1999, 181:2465-2471.
30. Llop P., Caruso P., Cubero J., Morente C., Lopez M.M. A simple extraction procedure for efficient routine detection of pathogenic bacteria in plant material by polymerase chain reaction. J. Microbiol. Methods 1999, 37:23-31.
31. Lorenz M.G., Wackernagel W. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Mol. Biol. Rev. 1994, 58:563-602.
32. Maiden M.C., Bygraves J.A., Feil E., Morelli G., Russell J.E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D.A., Feavers I.M., Achtman M., Spratt B.G. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 1998, 95:3140-3145.
33. Maiden M.C.J. Multilocus sequence typing of bacteria. Ann. Rev. Microbiol. 2006, 60:561-588.
34. Massomo S.M.S., Nielsen H., Mabagala R.B., Mansfeld-Giese K., Hockenhull J., Mortensen C.N. Identification and characterisation of Xanthomonas campestris pv. campestris strains from Tanzania by pathogenicity tests, Biolog, rep-PCR and fatty acid methyl ester analysis. Eur J Plant Pathol. 2003, 109:775-789.
35. Maynard-Smith J., Smith N.H. Detecting recombination from gene trees. Mol. Biol. Evol. 1998, 15:590-599.
36. Maynard-Smith J., Smith N.H., O'Rourke M., Spratt B.G. How clonal are bacteria?. Proc. Natl. Acad. Sci. USA 1993, 90:4384-4388.
37. McCulloch L. A bacterial leaf spot of horse-radish caused by Bacterium campestre var. armoraciae n. var. J. Agric. Res. 1929, 38:269-287.
38. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 1986, 3:418-426.
39. Parkinson N., Aritua V., Heeney J., Cowie C., Bew J., Stead D. Phylogenetic analysis of Xanthomonas species by comparison of partial gyrase B gene sequences. Int J Syst. Evol. Microbiol. 2007, 57:2881-2887.
40. Patil P., Bogdanove A., Sonti R. 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. 2007, 7:243.
41. Posada D., Crandall K.A. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
42. Rademaker J.L.W., Louws F.J., Schultz M.H., Rossbach U., Vauterin L., Swings J., de Bruijn F.J. A comprehensive species to strain taxonomic framework for Xanthomonas. Phytopathology 2005, 95:1098-1111.
43. Rozas J., Sánchez-DelBarrio J.C., Messeguer X., Rozas R. DnaSP: DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
44. Sarkar S.F., Guttman D.S. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 2004, 70:1999-2012.
45. Scally M., Schuenzel E.L., Stouthamer R., Nunney L. Multilocus sequence type system for the plant pathogen Xylella fastidiosa and relative contributions of recombination and point mutation to clonal diversity. Appl. Environ. Microbiol. 2005, 71:8491-8499.
46. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114-1116.
47. Solcà N.M., Bernasconi M.V., Valsangiacomo C., Van Doorn L.J., Piffaretti J.C. Population genetics of Helicobacter pylori in the southern part of Switzerland analysed by sequencing of four housekeeping genes (atpD, glnA, scoB and recA), and by vacA, cagA, iceA and IS605 genotyping. Microbiology 2001, 147:1693-1707.
48. Spratt B.G., Hanage W.P., Li B., Aanensen D.M., Feil E.J. Displaying the relatedness among isolates of bacterial species - the eBURST approach. FEMS Microbiol. Lett. 2004, 241:129-134.
49. Suerbaum S., Achtman M. Evolution of Helicobacter pylori: the role of recombination. Trends Microbiol. 1999, 7:182-184.
50. Thieme F., Koebnik 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., Ruckert C., Rupp O., Schneiker S., Schuster S.C., Vorholter F.J., Weber E., Puhler A., Bonas U., Bartels D., Kaiser O. Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence. J. Bacteriol. 2005, 187:7254-7266.
51. Vauterin L., Hoste B., Kersters K., Swings J. Reclassification of Xanthomonas. Int. J. Syst. Bacteriol. 1995, 45:472-489.
52. Vicente J.G., Conway J., Roberts S.J., Taylor J.D. Identification and origin of Xanthomonas campestris pv. campestris race and related pathovars. Phytopathology 2001, 91:492-499.
53. Vicente J.G., Everett B., Roberts S.J. Identification of isolates that cause a leaf spot disease of brassicas as Xanthomonas campestris pv. raphani and pathogenic and genetic comparison with related pathovars. Phytopathology 2006, 96:735-745.
54. Vos M., Velicer G.J. Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale. Appl. Environ. Microbiol. 2006, 72:3615-3625.
55. White H.E. Bacterial spot of radish and turnip. Phytopathology 1930, 20:653-662.
56. Williams P.H. Black rot: a continuing threat to world crucifers. Plant Dis. 1980, 64:736-745.
57. Yan S., Liu H., Mohr T.J., Jenrette J., Chiodini R., Zaccardelli M., Setubal J.C., Vinatzer B.A. Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Appl. Environ. Microbiol. 2008, 74:3171-3181.
58. Young J.M., Dye D.W., Bradbury J.F., Panagopoulos C.G., Robbs C.F. A proposed nomenclature and classification for plant pathogenic bacteria. N. Z. J. Agric. Res. 1978, 21:153-177.
59. Young J.M., Park D.-C., Shearman H.M., Fargier E. A multilocus sequence analysis of the genus Xanthomonas. Syst. Appl. Microbiol. 2008, 31:366-377.
60. Zhao Y., Damicone J.P., Demezas D.H., Bender C.L. Bacterial leaf spot diseases of leafy crucifers in oklahoma caused by pathovars of Xanthomonas campestris. Plant Dis. 2000, 84:1008-1014.
61. Zmasek C.M., Eddy S.R. ATV: display and manipulation of annotated phylogenetic trees. Bioinformatics 2001, 17:383-384.