Housekeeping gene sequencing and multilocus variable-number tandem-repeat analysis to identify subpopulations within Pseudomonas syringae pv. maculicola and Pseudomonas syringae pv. tomato that correlate with host specificity

Applied and Environmental Microbiology

Volumn 78, Issue 9, 2012, Pages 3266-3279

  Gironde, S ^a   Manceau, C ^a  

^a UNIVERSITÉ D'ANGERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BRASSICACEAE; EPIDEMIOLOGICAL STUDIES; GENE SEQUENCES; GENETIC STRUCTURE; HOST-SPECIFICITY; HOUSEKEEPING GENE; MINISATELLITE; PHYLOGENETIC ANALYSIS; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS; TOMATO PLANTS;

BACTERIA; GENES; PLATINUM;

FRUITS;

BACTERIAL DNA; DNA DIRECTED RNA POLYMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); MICROSATELLITE DNA;

BACTERIAL DISEASE; BACTERIUM; CORRELATION; DISEASE SEVERITY; EPIDEMIOLOGY; FRUIT; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC MARKER; GENETIC STRUCTURE; HOST RANGE; HOST SPECIFICITY; PATHOGENICITY; SUBPOPULATION;

ARTICLE; BRASSICACEAE; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ESSENTIAL GENE; FRANCE; GENETICS; HOST RANGE; MICROBIOLOGY; MOLECULAR GENETICS; MOLECULAR TYPING; NUCLEOTIDE SEQUENCE; PLANT DISEASE; PSEUDOMONAS SYRINGAE; TOMATO; VARIABLE NUMBER OF TANDEM REPEAT;

BRASSICACEAE; DNA GYRASE; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; FRANCE; GENES, ESSENTIAL; HOST SPECIFICITY; LYCOPERSICON ESCULENTUM; MICROSATELLITE REPEATS; MINISATELLITE REPEATS; MOLECULAR SEQUENCE DATA; MOLECULAR TYPING; PLANT DISEASES; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS, DNA;

FRANCE; LOIRE VALLEY;

BACTERIA (MICROORGANISMS); BRASSICACEAE; LYCOPERSICON ESCULENTUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. MACULICOLA; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 84861123507     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06655-11     Document Type: Article

References (60)

1. Ait Tayeb L, Ageron E, Grimont F, Grimont PAD. 2005. Molecular phylogeny of the genus Pseudomonas based on rpoB sequences and application for the identification of isolates. Res. Microbiol. 156:763-773.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Bouchouicha R, et al. 2009. Comparison of the performances of MLVA vs. the main other typing techniques for Bartonella henselae. Clin. Microbiol. Infect. 15:104-105.
4. Buell CR, et al. 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.
5. Bull CT, et al. 2010 Pseudomonas cannabina pv. cannabina pv. nov., and Pseudomonas cannabina pv. alisalensis (Cintas Koike and Bull, 2000) comb. nov., are members of the emended species Pseudomonas cannabina (ex Sutic & Dowson 1959) Gardan, Shafik, Belouin, Brosch, Grimont & Grimont 1999. Syst. Appl. Microbiol. 33:105-115.
6. Reference deleted.
7. Chang JH, Rathjen JP, Bernal AJ, Staskawicz BJ, Michelmore RW. 2000. avrPto enhances growth and necrosis caused by Pseudomonas syringae pv. tomato in tomato lines lacking either Pto or Prf. Mol. Plant Microbe Interact. 13:568-571.
8. Clerc A, Manceau C, Nesme X. 1998. Comparison of randomly amplified polymorphic DNA with amplified fragment length polymorphism to assess genetic diversity and genetic relatedness within genospecies III of Pseudomonas syringae. Appl. Environ. Microbiol. 64:1180-1187.
9. Cuppels DA. 1986. Generation and characterization of Tn5 insertion mutations in Pseudomona syringae pv. tomato. Appl. Environ. Microbiol. 51:323-327.
10. Cuppels DA, Ainsworth T. 1995. Molecular and physiological characterization of Pseudomonas syringae pv. tomato and Pseudomonas syringae pv. maculicola strains that produce the phytotoxin coronatine. Appl. Environ. Microbiol. 61:3530-3536.
11. Davis KR, Schott E, Ausubel FM. 1991. Virulence of selected phytopathogenic pseudomonads in Arabidopsis thaliana. Mol. Plant Microbe Interact. 4:477-488.
12. Dye DW, et al. 1980. International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. Rev. Plant Pathol. 59:153-168.
13. Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611-2620.
14. Fischer-Le Saux M, et al. 2008. Apports du séquençage multiloci à la phylogénie et à la taxonomie de deux genres majeurs de bactéries phytopathogènes: Pseudomonas et Xanthomonas, p 171-185. Les Actes du BRG, vol 7. Fondation pour la Recherche sur la Biodiversité, Paris, France.
15. Gardan L, et al. 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int. J. Syst. Bacteriol. 49(PT 2):469-478.
16. Goudet J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86:485-486.
17. Hajri A, et al. 2009. A "repertoire for repertoire" hypothesis: repertoires of type three effectors are candidate determinants of host specificity Xanthomonas. PLoS One. doi:10.1371/annotation/92d243d0-22b2-44da-9618-83b4aa252724.
18. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
19. Hanekamp T, Kobayashi D, Hayes S, Stayton MM. 1997. Avirulence geneDof Pseudomonas syringae pv. tomato may have undergone horizontal gene transfer. FEBS Lett. 415:40-44.
20. Hendson M, Hildebrand DC, Schroth MN. 1992. Relatedness of Pseudomonas syringae pv. tomato, Pseudomonas syringae pv. maculicola and Pseudomonas syringae pv. antirrhini. J. Appl. Bacteriol. 73:455-464.
21. Hildebrand DC, Schroth MN, Sand DC. 1988. Pseudomonas. In Schaad NW(ed), Laboratory guide for identification of plant pathogenic bacteria, 2nd ed. American Phytopathological Society, St. Paul, MN.
22. Hurlbert SH. 1971. The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577-586.
23. Hwang MSH, Morgan RL, Sarkar SF, Wang PW, Guttman DS. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 71:5182-5191.
24. Joardar V, Lindeberg M, Schneider DJ, Collmer A, Buell CR. 2005. Lineage-specific regions in Pseudomonas syringae pv. tomato DC3000. Mol. Plant Pathol. 6:53-64.
25. Kearney B, Ronald PC, Dahlbeck D, Staskawicz BJ. 1988. Molecular basis for evasion of plant host defense in bacterial spot disease of pepper. Nature 332:541-543.
26. Kearney B, Staskawicz BJ. 1990. Characterization of IS476 and its role in bacterial spot disease of tomato and pepper. J. Bacteriol. 172:143-148.
27. Kim JF, Charkowski AO, Alfano JR, Collmer A, Beer SV. 1998. Sequences related to transposable elements and bacteriophages flank avirulence genes of Pseudomonas syringae. Mol. Plant Microbe Interact. 11: 1247-1252.
28. Kim YJ, Lin N-C, Martin GB. 2002. Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589-598.
29. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
30. King EO, Ward MK, Raney DE. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Clin. Med. 44:301-307.
31. Kobayashi DY, Tamaki SJ, Keen NT. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. U. S. A. 86:157-161.
32. Le Flèche P, et al. 2001. A tandem repeats database for bacterial genomes: application to the genotyping of Yersinia pestis and Bacillus anthracis. BMC Microbiol. 1:2.
33. Lin NC, Abramovitch RB, Mm YJ, Martin GB. 2006. Diverse AvrPtoB homologs from several Pseudomonas syringae pathovars elicit Ptodependent resistance and have similar virulence activities. Appl. Environ. Microbiol. 72:702-712.
34. Lin NC, Martin GB. 2005. An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol. Plant Microbe Interact. 18:43-51.
35. Lindeberg M, Myers CR, Collmer A, Schneider DJ. 2008. Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Mol. Plant Microbe Interact. 21:685-700.
36. Lindstedt BA. 2005. Multiple-locus variable number tandem repeats analysis for genetic fingerprinting of pathogenic bacteria. Electrophoresis 26:2567-2582.
37. Ma WB, Dong FFT, Stavrinides J, Guttman DS. 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PloS Genet. 2:2131-2142.
38. Mahillon J, Chandler M. 1998. Insertion sequences. Microbiol. Mol. Biol. Rev. 62:725-774.
39. Mahillon J, Leonard C, Chandler M. 1999. IS elements as constituents of bacterial genomes. Res. Microbiol. 150:675-687.
40. Manceau C, Horvais A. 1997. Assessment of genetic diversity among strains of Pseudomonas syringae by PCR-restriction fragment length polymorphism analysis of rRNA operons with special emphasis on P. syringae pv. tomato. Appl. Environ. Microbiol. 63:498-505.
41. Ngoc LBT, et al. 2009. From local surveys to global surveillance: three high-throughput genotyping methods for epidemiological monitoring of Xanthomonas citri pv. citri pathotypes. Appl. Environ. Microbiol. 75: 1173-1184.
42. Parkinson N, Bryant R, Bew J, Elphinstone J. 2010. Rapid phylogenetic identification of members of the Pseudomonas syringae species complex using the rpoD locus. Plant Pathol. 60:338-344.
43. Poussier S, et al. 2003. Host plant-dependent phenotypic reversion of Ralstonia solanacearum from non-pathogenic to pathogenic forms via alterations in the phcA gene. Mol. Microbiol. 49:991-1003.
44. Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
45. Radomski N, et al. 2010. Determination of genotypic diversity of Mycobacterium avium subspecies from human and animal origins by mycobac-terial interspersed repetitive-unit-variable-number tandem-repeat and IS1311 restriction fragment length polymorphism typing methods. J. Clin. Microbiol. 48:1026-1034.
46. Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ. 1992. The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174:1604-1611.
47. Saitou N, Nei M. 1987. The neighbor-joining method-a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
48. Sarkar SF, Gordon JS, Martin GB, Guttman DS. 2006. Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 174:1041-1056.
49. Sarkar SF, Guttman DS. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 70:1999-2012.
50. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 34:D32-D36.
51. Takikawa Y, Nishiyama N, Okba K, Tsuyumu S, Goto M. 1992. Synonymy of Pseudomonas syringae pv. maculicola and Pseudomonas syringae pv. tomato, p 199-204. In Lemattre SFM, Rudolph K, Swings JG (ed), Plant pathogenic bacteria, vol 66. INRA, Versailles, France.
52. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
53. Teh CSJ, Chua KH, Thong KL. 2010. Multiple-locus variable-number tandem repeat analysis of Vibrio cholerae in comparison with pulsed field gel electrophoresis and virulotyping. J. Biomed. Biotechnol. doi:10.1155/2010/ 817190.
54. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
55. Tien YY, Wang YW, Tung SK, Liang SY, Chiou CS. 2011. Comparison of multilocus variable-number tandem repeat analysis and pulsed-field gel electrophoresis in molecular subtyping of Salmonella enterica serovars Paratyphi A. Diagn. Microbiol. Infect. Dis. 69:1-6.
56. Top J, Schouls LM, Bonten MJM, Willems RJL. 2004. Multiple-locus variable-number tandem repeat analysis, a novel typing scheme to study the genetic relatedness and epidemiology of Enterococcus faecium isolates. J. Clin. Microbiol. 42:4503-4511.
57. Yamamoto S, et al. 2000. Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiology 146(Pt 10):2385-2394.
58. Yan S, et al. 2008. Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Appl. Environ. Microbiol. 74:3171-3181.
59. Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF. 1978. Proposed nomenclature and classification for plant pathogenic bacteria. New Zealand J. Agric. Res. 21:153-177.
60. Zhao Y, Damicone JP, Demezas DH, Rangaswamy V, Bender CL. 2000. Bacterial leaf spot of leafy crucifers in Oklahoma caused by Pseudomonas syringae pv. maculicola. Plant Dis. 84:1015-1020.