Comparative Genomics of Multiple Strains of Pseudomonas cannabina pv. alisalensis, a Potential Model Pathogen of Both Monocots and Dicots

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Sarris, Panagiotis F ^a,b,i   Trantas, Emmanouil A ^a   Baltrus, David A ^c   Bull, Carolee T ^d   Wechter, William Patrick ^e   Yan, Shuangchun ^f   Ververidis, Filippos ^a   Almeida, Nalvo F ^g   Jones, Corbin D ^h   Dangl, Jeffery L ^h   Panopoulos, Nickolas J ^b,j   Vinatzer, Boris A ^f   Goumas, Dimitrios E ^a  

^a TECHNOLOGICAL EDUCATIONAL INSTITUTE OF CRETE   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c UNIVERSITY OF ARIZONA   (United States)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e Virginia Tech ^*  (United States)

^f VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^g FEDERAL UNIVERSITY OF MATO GROSSO DO SUL   (Brazil)

^h UNIVERSITY OF NORTH CAROLINA   (United States)

ⁱ SAINSBURY LABORATORY   (United Kingdom)

^j UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN HRC; PROTEIN HRCN; PROTEIN HRCQA; PROTEIN HRCQB; PROTEIN HRCR; PROTEIN HRCS; PROTEIN HRCT; PROTEIN HRCU; PROTEIN HRCV; PROTEIN HRP; PROTEIN HRPA; PROTEIN HRPB; PROTEIN HRPC; PROTEIN HRPD; PROTEIN HRPE; PROTEIN HRPF; PROTEIN HRPG; PROTEIN HRPJ; PROTEIN HRPK; PROTEIN HRPL; PROTEIN HRPO; PROTEIN HRPP; PROTEIN HRPQ; PROTEIN HRPR; PROTEIN HRPS; PROTEIN HRPT; PROTEIN HRPV; PROTEIN HRPZ; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; COMPARATIVE STUDY; CONTROLLED STUDY; DICOT; GENE CLUSTER; GENE LOCATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOMIC ISLAND; HOST RANGE; HRC GENE; HRP GENE; MOLECULAR EVOLUTION; MONOCOT; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOTYPE; PHYLOGENY; PLANT DISEASE; PREDICTION; PROTEIN LOCALIZATION; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS CANNABINA; PSEUDOMONAS SYRINGAE; SEED PLANT; SEQUENCE ANALYSIS; STRAIN DIFFERENCE; TYPE III SECRETION SYSTEM; TYPE VI SECRETION SYSTEM;

AVENA SATIVA; BACTERIAL PROTEINS; BROMUS; CHROMOSOME MAPPING; GENOME, BACTERIAL; GENOMIC ISLANDS; GENOMICS; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MULTIGENE FAMILY; PHYLOGENY; PLANT DISEASES; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

DICOTYLEDONEAE; LILIOPSIDA; PSEUDOMONAS CANNABINA; PSEUDOMONAS SYRINGAE;

EID: 84875518633     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059366     Document Type: Article

References (69)

1. Sutic D, Dowson WJ, (1959) An investigation of a serious disease of hemp (Cannabis sativa L.) in Yugoslavia. Phytopath Z 34: 307-314.
2. Gardan L, Shafik H, Belouin S, Broch R, Grimont F, 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: 469-478.
3. Bull CT, Manceau C, Lydon J, Kong H, Vinatzer BA, 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.
4. Bull CT, Rubio I, (2011) First report of bacterial blight of crucifers caused by Pseudomonas cannabina pv. alisalensis in Australia. Plant Dis 95: 1027-1027.
5. Williams PH, Keen NT, (1966) Bacterial blight of radish. Plant Dis Rep 50: 192-195.
6. Hendrickson EL, Guevera P, Penaloza-Vazquez A, Shao J, Bender C, et al. (2000) Virulence of the phytopathogen Pseudomonas syringae pv. maculicola is rpoN dependent. J Bacteriol 182: 3498-3507.
7. Cui J, Jander G, Racki LR, Kim PD, Pierce NE, et al. (2002) Signals involved in Arabidopsis resistance to Trichoplusia in caterpillars induced by virulent and avirulent strains of the phytopathogen Pseudomonas syringae. Plant Physiol 129: 551-564.
8. Wang L, Mitra RM, Hasselmann KD, Sato M, Lenarz-Wyatt L, et al. (2008) The genetic network controlling the Arabidopsis transcriptional response to Pseudomonas syringae pv. maculicola: roles of major regulators and the phytotoxin coronatine. Mol Plant Microbe Interact 21: 1408-1420.
9. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, et al. (2002) A functional screen for the Type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726.
10. Sarris PF, Karri IV, Goumas DE (2010) First report of Pseudomonas syringae pv. alisalensis causing bacterial blight of arugula (Eruca vesicaria subsp. sativa) in Greece. New Disease Reports 22.
11. Bull CT, du Toit LJ, (2008) First report of bacterial blight on conventionally and organically grown Arugula in Nevada caused by Pseudomonas syringae pv. alisalensis. Plant Dis 93: 109-109.
12. Bull CT, Goldman P, Koike ST, (2004) Bacterial blight on arugula, a new disease caused by Pseudomonas syringae pv. alisalensis in California. Plant Dis 88: 1384-1384.
13. Mauzey SJ, Koike ST, Bull CT, (2010) First report of bacterial blight of cabbage (Brassica oleracea var. capitata) caused by Pseudomonas cannabina pv. alisalensis in California. Plant Dis 95: 71-71.
14. Koike ST, Kammeijer K, Bull CT, O'Brien D, (2006) First report of bacterial blight of Romanesco cauliflower (Brassica oleracea var. botrytis) caused by Pseudomonas syringae pv. alisalensis in California. Plant Dis 90: 1551-1551.
15. Bull CT, Mauzey SJ, Koike ST, (2010) First report of bacterial blight of brussels sprouts (Brassica oleracea var. gemmifera) caused by Pseudomonas cannabina pv. alisalensis in California. Plant Dis 94: 1375-1375.
16. Koike ST, Kammeijer K, Bull CT, O'Brien D, (2007) First report of bacterial blight of Rutabaga (Brassica napus var. napobrassica) caused by Pseudomonas syringae pv. alisalensis in California. Plant Dis 91: 112-112.
17. Rubio I, Hiddink G, Asma M, Bull CT, (2012) First report of the crucifer pathogen Pseudomonas cannabina pv. alisalensis causing bacterial blight on Radish (Raphanus sativus) in Germany. Plant Dis 96: 904-904.
18. Cintas NA, Koike ST, Bull CT, (2002) A new pathovar, Pseudomonas syringae pv. alisalensis pv. nov., proposed for the causal agent of bacterial blight of broccoli and broccoli raab. Plant Dis 86: 992-998.
19. Dale C, Moran NA, (2006) Molecular interactions between bacterial symbionts and their hosts. Cell 126: 453-465.
20. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF, et al. (2010) Playing the Harp: Evolution of our understanding of hrp/hrc genes. Annu Rev Phytopathol.
21. Troisfontaines P, Cornelis GR, (2005) Type III Secretion: More systems than you think. Physiology 20: 326-339.
22. Abby SS, Rocha EP, (2012) The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems. PLoS Genet 8: e1002983.
23. Sarris P, Skandalis N, Kokkinidis M, Panopoulos N, (2010) In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Mol Plant Pathol 11: 795-804.
24. Sarris PF, Trantas EA, Skandalis N, Tampakaki AP, Kapanidou M, et al. (2012) Phytobacterial type VI Secretion System- Gene distribution, Phylogeny, Structure and Biological functions. In: Cumagun CJ, editor. Plant Pathol: InTech.
25. Haapalainen M, Mosorin H, Dorati F, Wu R-F, Roine E, et al. (2012) Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for competitive fitness against bacteria and yeasts. J Bacteriol.
26. Ahmed N, (2009) A Flood of microbial genomes-Do we need more? PLoS ONE 4: e5831.
27. 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 of the United States of America 100: 10181-10186.
28. Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, et al. (2008) A Draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a Type III Effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe In 22: 52-62.
29. 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. J Bacteriol 187: 6488-6498.
30. 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 of the United States of America 102: 11064-11069.
31. Sohn KH, Jones JD, Studholme DJ, (2012) Draft genome sequence of Pseudomonas syringae pathovar syringae strain FF5, causal agent of stem tip dieback disease on ornamental pear. J Bacteriol 194: 3733-3734.
32. Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, et al. (2009) De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res 19: 294-305.
33. Studholme D, Ibanez S, MacLean D, Dangl J, Chang J, et al. (2009) A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudomonas syringae pathovar tabaci 11528. BMC Genomics 10: 395.
34. Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, et al. (2010) Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS ONE 5: e10224.
35. Rodriguez-Palenzuela P, Matas IM, Murillo J, Lopez-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. Environ Microbiol 12: 1604-1620.
36. Qi M, Wang D, Bradley CA, Zhao Y, (2011) Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine pseudomonads. PLoS ONE 6: e16451.
37. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, et al. (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS pathog 7: e1002132.
38. Stavrinides J, Guttman DS, (2004) Nucleotide sequence and evolution of the five-plasmid complement of the phytopathogen Pseudomonas syringae pv. maculicola ES4326. J Bacteriol 186: 5101-5115.
39. Keinath A, Wechter W, Smith J, (2006) First report of bacterial leaf spot on leafy Brassica greens caused by Pseudomonas syringae pv. maculicola in South Carolina. Plant Dis 90: 683-683.
40. Darling ACE, Mau B, Blattner FR, Perna NT, (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 1394-1403.
41. Cunnac S, Lindeberg M, Collmer A, (2009) Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr Opin Microbiol 12: 53-60.
42. Bronstein PA, Marrichi M, Cartinhour S, Schneider DJ, DeLisa MP, (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.
43. Guttman DS, Gropp SJ, Morgan RL, Wang PW, (2006) Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Mol Biol Evol 23: 2342-2354.
44. Souza RC, del Rosario Quispe Saji G, Costa MO, Netto DS, Lima NC, et al. (2012) AtlasT4SS: a curated database for type IV secretion systems. BMC Microbiol 12: 172.
45. Tegli S, Gori A, Cerboneschi M, Cipriani MG, Sisto A, (2011) Type three secretion system in Pseudomonas savastanoi pathovars: does timing matter? Genes 2: 957-979.
46. Preston GM, Collmer A (2004) The Type III Secretion Systems of plant-associated Pseudomonads: Genes and Proteins on the move. In: Ramos J-L, editor. Pseudomonas: Virulence and gene regulation. New York: Plenum Pub Corp. 181-222.
47. Bull CT, Clarke CR, Cai R, Vinatzer BA, Jardini TM, et al. (2011) Multilocus sequence typing of Pseudomonas syringae sensu lato confirms previously described genomospecies and permits rapid identification of P. syringae pv. coriandricola and P. syringae pv. apii causing bacterial leaf spot on parsley. Phytopathology 101: 847-858.
48. 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.
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. Naum M, Brown EW, Mason-Gamer RJ, (2009) Phylogenetic evidence for extensive horizontal gene transfer of type III secretion system genes among enterobacterial plant pathogens. Microbiology 155: 3187-3199.
51. Inoue Y, Takikawa Y, (2006) The hrpZ and hrpA genes are variable, and useful for grouping Pseudomonas syringae bacteria. Journal of General Plant Pathology 72: 26-33.
52. Sarris PF, Gao S, Karademiris K, Jin H, Kalantidis K, et al. (2011) Phytobacterial type III effectors HopX1, HopAB1 and HopF2 enhance sense-post-transcriptional gene silencing independently of plant R gene-effector recognition. Mol Plant Microbe Interact 24: 907-917.
53. Sarris PF, Scoulica EV, (2011) Pseudomonas entomophila and Pseudomonas mendocina: Potential models for studying the bacterial type VI secretion system. Infect Genet Evol 11: 1352-1360.
54. Barret M, Egan F, Fargier E, Morrissey JP, O'Gara F, (2011) Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology 157: 1726-1739.
55. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7: 25-37.
56. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
57. Cai R, Lewis J, Yan S, Liu H, Clarke CR, et al. (2011) The plant pathogen Pseudomonas syringae pv. tomato Is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 7: e1002130.
58. Zerbino DR, Birney E, (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821-829.
59. Thompson JD, Higgins DG, Gibson TJ, (1994) Clustal-W- 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.
60. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
61. Felsenstein J, (1985) Confidence-Limits on Phylogenies- an Approach Using the Bootstrap. Evolution 39: 783-791.
62. Tamura K, Nei M, Kumar S, (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America 101: 11030-11035.
63. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
64. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
65. Li L, Stoeckert CJ Jr, Roos DS, (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
66. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
67. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
68. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
69. Cintas NA, Koike ST, Bull CT (2000) Rappini bacterial blight declines with delayed replanting in the Salinas Valley of California; New Orleans, Louisiana. S15.