Miniature transposable sequences are frequently mobilized in the bacterial plant pathogen Pseudomonas syringae pv. phaseolicola

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Bardaji, Leire ^a   Añorga, Maite ^a   Jackson, Robert W ^b   Martínez Bilbao, Alejandro ^a   Yanguas Casás, Natalia ^a   Murillo, Jesús ^a  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BEAN; CHROMOSOME ANALYSIS; CONTROLLED STUDY; DNA TRANSPOSITION; GENE FREQUENCY; GENE IDENTIFICATION; GENE INSERTION SEQUENCE; GENE SEQUENCE; GENE VECTOR; GENETIC RECOMBINATION; GENOMIC FRAGMENT; HETEROZYGOTE; IN VIVO STUDY; INVERTED REPEAT; MOLECULAR CLONING; MOLECULAR SIZE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSCILLATION; PLASMID; PSEUDOMONAS SYRINGAE; SACB GENE; TRANSPOSON; BACTERIAL GENOME; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT;

ACARI; BACTERIA (MICROORGANISMS); PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. PHASEOLICOLA;

BASE SEQUENCE; DNA TRANSPOSABLE ELEMENTS; GENETIC VECTORS; GENOME, BACTERIAL; INVERTED REPEAT SEQUENCES; MOLECULAR SEQUENCE ANNOTATION; PLANTS; PSEUDOMONAS SYRINGAE;

EID: 80053919660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025773     Document Type: Article

References (71)

1. Siguier P, Filee J, Chandler M, (2006) Insertion sequences in prokaryotic genomes. Current Opinion in Microbiology 9: 526-531.
2. Mahillon J, Chandler M, (1998) Insertion sequences. Microbiology and Molecular Biology Reviews 62: 725-774.
3. Jackson RW, Vinatzer B, Arnold DL, Dorus S, Murillo J, (2011) The influence of the accessory genome on bacterial pathogen evolution. Mobile Genetic Elements 1: 55-65.
4. Craig NL, Craigie R, Gellert M, Lambowitz AM, eds. (2002) (2002) Mobile DNA II Washington, D.C. ASM Press.
5. McEvoy CRE, Falmer AA, van Pittius NCG, Victor TC, van Helden PD, et al. (2007) The role of IS6110 in the evolution of Mycobacterium tuberculosis. Tuberculosis 87: 393-404.
6. Sundin GW, Murillo J, (2009) Gene traders: characteristics of native plasmids from plant pathogenic bacteria. In: Jackson RW, editors. Plant pathogenic bacteria: genomics and molecular biology Cambs Caister Academic Press pp. 295-310.
7. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M, (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Research 34: D32-D36.
8. Bertels F, Rainey PB, (2011) Within-genome evolution of REPINs: a new family of miniature mobile DNA in bacteria. PLoS Genetics 7: e1002132.
9. Delihas N, (2008) Small mobile sequences in bacteria display diverse structure/function motifs. Molecular Microbiology 67: 475-481.
10. Mansfield JW, (2009) From bacterial avirulence genes to effector functions via the hrp delivery system: an overview of 25 years of progress in our understanding of plant innate immunity. Molecular Plant Pathology 10: 721-734.
11. Young JM, (2010) Taxonomy of Pseudomonas syringae. Journal of Plant Pathology 92: S5-S14.
12. Sarkar SF, Guttman DS, (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Applied and Environmental Microbiology 70: 1999-2012.
13. Sarkar SF, Gordon JS, Martin GB, Guttman DS, (2006) Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 174: 1041-1056.
14. Kim JF, Charkowski AO, Alfano JR, Collmer A, Beer SV, (1998) Transposable elements and bacteriophage sequences flanking Pseudomonas syringae avirulence genes. Molecular Plant-Microbe Interactions 11: 1247-1252.
15. Arnold DL, Jackson RW, Fillingham AJ, Goss SC, Taylor JD, et al. (2001) Highly conserved sequences flank avirulence genes: isolation of novel avirulence genes from Pseudomonas syringae pv. pisi. Microbiology 147: 1171-1182.
16. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, et al. (1999) Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proceedings of the National Academy of Sciences USA 96: 10875-10880.
17. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, et al. (2005) Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. Journal of Bacteriology 187: 6488-6498.
18. Rodríguez-Palenzuela P, Matas I, Murillo J, López-Solanilla E, Bardaji L, et al. (2010) Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Environmental Microbiology 12: 1604-1620.
19. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences USA 100: 10181-10186.
20. Vivian A, Murillo J, Jackson RW, (2001) The role of plasmids in phytopathogenic bacteria: mobile arsenals? Microbiology 147: 763-780.
21. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, et al. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proceedings of the National Academy of Sciences USA 102: 11064-11069.
22. Sundin GW, (2007) Genomic insights into the contribution of phytopathogenic bacterial plasmids to the evolutionary history of their hosts. Annual Review of Phytopathology 45: 129-151.
23. Yamada T, Lee PD, Kosuge T, (1986) Insertion sequence elements of Pseudomonas savastanoi: Nucleotide sequence and homology with Agrobacterium tumefaciens transfer DNA. Proceedings of the National Academy of Sciences USA 83: 8263-8267.
24. Romantschuk M, Richter GY, Mukhopadhyay P, Mills D, (1991) IS801, an insertion sequence element isolated from Pseudomonas syringae pathovar phaseolicola. Molecular Microbiology 5: 617-622.
25. Kamiunten H, Inoue S, Yakabe Y, Iida S, (2002) Characterization of ISPsy2 and ISPsy3, newly identified insertion sequences in Pseudomonas syringae pv. eriobotryae. Journal of General Plant Pathology 68: 75-80.
26. Landgraf A, Weingart H, Tsiamis G, Boch J, (2006) Different versions of Pseudomonas syringae pv. tomato DC3000 exist due to the activity of an effector transposon. Molecular Plant Pathology 7: 355-364.
27. Arnold DL, Lovell HC, Jackson RW, Mansfield JW, (2011) Pseudomonas syringae pv. phaseolicola: from 'has bean' to supermodel. Molecular Plant Pathology 12: 617-627.
28. Lovell HC, Jackson RW, Mansfield JW, Godfrey SAC, Hancock JT, et al. (2011) In planta conditions induce genomic changes in Pseudomonas syringae pv. phaseolicola. Molecular Plant Pathology 12: 167-176.
29. Oguiza JA, Rico A, Rivas LA, Sutra L, Vivian A, et al. (2004) Pseudomonas syringae pv. phaseolicola can be separated into two genetic lineages distinguished by the possession of the phaseolotoxin biosynthetic cluster. Microbiology 150: 473-482.
30. Führer ME, Navarro de la Fuente L, Rivas L, Hernández-Flores JL, Garcidueñas-Piña R, et al. (2008) Genetic relatedness among the different lineages of Pseudomonas syringae pv. phaseolicola. In: Fatmi M, Collmer A, Iacobellis NS, Mansfield JW, Murillo J, editors. Pseudomonas syringae pathovars and related pathogens Identification, epidemiology and genomics Dordrecht Springer pp. 175-182.
31. Stevens C, Bennett MA, Athanassopoulos E, Tsiamis G, Taylor JD, et al. (1998) Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Molecular Microbiology 29: 165-177.
32. Rivas LA, Mansfield J, Tsiamis G, Jackson RW, Murillo J, (2005) Changes in race-specific virulence in Pseudomonas syringae pv. phaseolicola are associated with a chimeric transposable element and rare deletion events in a plasmid-borne pathogenicity island. Applied and Environmental Microbiology 71: 3778-3785.
33. Szabo LJ, Mills D, (1984) Integration and excision of pMC7105 in Pseudomonas syringae pv. phaseolicola: involvement of repetitive sequences. Journal of Bacteriology 157: 821-827.
34. Garcillán-Barcia MP, de la Cruz F, (2002) Distribution of IS91 family insertion sequences in bacterial genomes: evolutionary implications. FEMS Microbiology Ecology 42: 303-313.
35. Garcillán-Barcia MP, Bernales I, Mendiola MV, de la Cruz F, (2002) IS91 rolling-circle transposition. In: Craig NL, Craigie R, Gellert M, Lambowitz AM, editors. Mobile DNA II Washington, D.C. ASM Press pp. 891-904.
36. Richter GY, Björklöf K, Romantschuk M, Mills D, (1998) Insertion specificity and trans-activation of IS801. Molecular and General Genetics 260: 381-387.
37. Bardaji L, Pérez-Martínez I, Rodríguez-Moreno L, Rodríguez-Palenzuela P, Sundin GW, et al. (2011) Sequence and role in virulence of the three plasmid complement of the model tumor-inducing bacterium Pseudomonas savastanoi pv. savastanoi NCPPB 3335. PLoS ONE in press.
38. Chen Y, Zhou F, Li G, Xu Y, (2009) MUST: A system for identification of miniature inverted-repeat transposable elements and applications to Anabaena variabilis and Haloquadratum walsbyi. Gene 436: 1-7.
39. Han Y, Wessler SR, (2010) MITE-Hunter: a program for discovering miniature inverted-repeat transposable elements from genomic sequences. Nucleic Acids Research 193: 4259-4260.
40. Ohtsubo Y, Genka H, Komatsu H, Nagata Y, Tsuda M, (2005) High-temperature-induced transposition of insertion elements in Burkholderia multivorans ATCC 17616. Applied and Environmental Microbiology 71: 1822-1828.
41. Gay P, Le Coq D, Steinmetz M, Berkelman T, Kado CI, (1985) Positive selection procedure for the entrapment of insertion sequences elements in gram-negative bacteria. Journal of Bacteriology 164: 918-921.
42. Nagy Z, Chandler M, (2004) Regulation of transposition in bacteria. Research in Microbiology 155: 387-398.
43. Drevinek P, Baldwin A, Lindenburg L, Joshi LT, Marchbank A, et al. (2010) Oxidative stress of Burkholderia cenocepacia induces insertion sequence-mediated genomic rearrangements that interfere with macrorestriction-based genotyping. Journal of Clinical Microbiology 48: 34-40.
44. Valle J, Vergara-Irigaray M, Merino N, Penades JR, Lasa I, (2007) σB regulates IS256-mediated Staphylococcus aureus biofilm phenotypic variation. Journal of Bacteriology 189: 2886-2896.
45. Touchon M, Rocha EPC, (2007) Causes of insertion sequences abundance in prokaryotic genomes. Molecular Biology and Evolution 24: 969-981.
46. Lindeberg M, Myers CR, Collmer A, Schneider DJ, (2008) Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Molecular Plant-Microbe Interactions 21: 685-700.
47. Wallden K, Rivera-Calzada A, Waksman G, (2010) Type IV secretion systems: versatility and diversity in function. Cellular Microbiology 12: 1203-1212.
48. Norman A, Hansen LH, Sørensen SJ, (2009) Conjugative plasmids: vessels of the communal gene pool. Philosophical Transactions of the Royal Society B: Biological Sciences 364: 2275-2289.
49. Mendiola MV, Bernales I, de la Cruz F, (1994) Differential roles of the transposon termini in IS91 transposition. Proceedings of the National Academy of Sciences USA 91: 1922-1926.
50. Toleman MA, Bennett PM, Walsh TR, (2006) ISCR elements: novel gene-capturing systems of the 21st century? Microbiology and Molecular Biology Reviews 70: 296-316.
51. Stavrinides J, Ma W, Guttman DS, (2006) Terminal reassortment drives the quantum evolution of type III effectors in bacterial pathogens. PLoS Pathogens 2: e104.
52. Yan S, Liu H, Mohr TJ, Jenrette J, Chiodini R, et al. (2008) Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Applied and Environmental Microbiology 74: 3171-3181.
53. Burt A, Trivers R, (2006) Genes in conflict: The biology of selfish genetic elements Cambridge, Massachusetts Belknap Press of Harvard University Press.
54. Zhou F, Tran T, Xu Y, (2008) Nezha, a novel active miniature inverted-repeat transposable element in cyanobacteria. Biochemical and Biophysical Research Communications 365: 790-794.
55. Robertson AE, Wechter WP, Denny TP, Fortnum BA, Kluepfel DA, (2004) Relationship between avirulence gene (avrA) diversity in Ralstonia solanacearum and bacterial wilt incidence. Molecular Plant-Microbe Interactions 17: 1376-1384.
56. Poirel L, Carrer A, Pitout JD, Nordmann P, (2009) Integron mobilization unit as a source of mobility of antibiotic resistance genes. Antimicrobial Agents and Chemotherapy 53: 2492-2498.
57. Stavrinides J, Guttman D, (2004) Nucleotide sequence and evolution of the five-plasmid complement of the phytopathogen Pseudomonas syringae pv. maculicola ES4326. Journal of Bacteriology 186: 5101-5115.
58. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory.
59. Teverson DM, (1991) Genetics of pathogenicity and resistance in the halo-blight disease of beans in Africa [Ph. D. Thesis] Birmingham, UK University of Birmingham.
60. Taylor JD, Teverson DM, Allen DJ, Pastor-Corrales MA, (1996) Identification and origin of races of Pseudomonas syringae pv. phaseolicola from Africa and other bean growing areas. Plant Pathology 45: 469-478.
61. King EO, Ward NK, Raney DE, (1954) Two simple media for the demonstration of pyocyanin and fluorescein. Journal of Laboratory and Clinical Medicine 44: 301-307.
62. Keane PJ, Kerr A, New. PB, (1970) Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Australian Journal of Biological Sciences 23: 585-595.
63. Cummings L, Riley L, Black L, Souvorov A, Resenchuk S, et al. (2002) Genomic BLAST: custom-defined virtual databases for complete and unfinished genomes. FEMS Microbiology Letters 216: 133-138.
64. Corpet F, (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16: 10881-10890.
65. Tatusova TA, Madden TL, (1999) BLAST 2 SEQUENCES, a new tool for comparing protein and nucleotide sequences. FEMS Microbiology Letters 174: 247-250.
66. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al. (2000) Artemis: sequence visualisation and annotation. Bioinformatics 16: 944-945.
67. Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, et al. (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422-3423.
68. Abbott JC, Aanensen DM, Rutherford K, Butcher S, Spratt BG, (2005) WebACT-an online companion for the Artemis Comparison Tool. Bioinformatics 21: 3665-3666.
69. Miché L, Fauré D, Blot M, Cabanne-Giuli E, Balandreau J, (2001) Detection and activity of insertion sequences in environmental strains of Burkholderia. Environmental Microbiology 3: 766-773.
70. Sesma A, Sundin GW, Murillo J, (1998) Closely related replicons coexisting in the phytopathogen Pseudomonas syringae show a mosaic organization of the replication region and altered incompatibility behavior. Applied and Environmental Microbiology 64: 3948-3953.
71. Harper S, Zewdie N, Brown IR, Mansfield JW, (1987) Histological, physiological and genetical studies of the responses of leaves and pods of Phaseolus vulgaris to three races of Pseudomonas syringae pv. phaseolicola and to Pseudomonas syringae pv. coronafaciens. Physiological and Molecular Plant Pathology 31: 153-172.