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PMID: 16159782 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition.

Journal of bacteriology ·Vol. 187 ·No. 18 ·2005-09-00 ·Pages 6488-98

Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, Deboy R, Durkin AS, Giglio MG, Madupu R, Nelson WC, Rosovitz MJ, Sullivan S, Crabtree J, Creasy T, Davidsen T, Haft DH, Zafar N, Zhou L, Halpin R, Holley T, Khouri H, Feldblyum T, White O, Fraser CM, Chatterjee AK, Cartinhour S, Schneider DJ, Mansfield J, Collmer A, Buell CR

Abstract

Pseudomonas syringae pv. phaseolicola, a gram-negative bacterial plant pathogen, is the causal agent of halo blight of bean. In this study, we report on the genome sequence of P. syringae pv. phaseolicola isolate 1448A, which encodes 5,353 open reading frames (ORFs) on one circular chromosome (5,928,787 bp) and two plasmids (131,950 bp and 51,711 bp). Comparative analyses with a phylogenetically divergent pathovar, P. syringae pv. tomato DC3000, revealed a strong degree of conservation at the gene and genome levels. In total, 4,133 ORFs were identified as putative orthologs in these two pathovars using a reciprocal best-hit method, with 3,941 ORFs present in conserved, syntenic blocks. Although these two pathovars are highly similar at the physiological level, they have distinct host ranges; 1448A causes disease in beans, and DC3000 is pathogenic on tomato and Arabidopsis. Examination of the complement of ORFs encoding virulence, fitness, and survival factors revealed a substantial, but not complete, overlap between these two pathovars. Another distinguishing feature between the two pathovars is their distinctive sets of transposable elements. With access to a fifth complete pseudomonad genome sequence, we were able to identify 3,567 ORFs that likely comprise the core Pseudomonas genome and 365 ORFs that are P. syringae specific.

MeSH Terms
Bacterial Proteins/genetics,physiology DNA, Bacterial/chemistry,genetics Genes, Bacterial Genome, Bacterial Molecular Sequence Data Pseudomonas syringae/classification,genetics,pathogenicity,physiology Species Specificity Virulence
Chemicals
Bacterial Proteins DNA, Bacterial
Authors & Affiliations
32 authors, click to expand affiliations / ORCID
Joardar Vinita
The Institute for Genomic Research, 9712 Medical Center Dr., Rockville, MD 20850, USA.
Lindeberg Magdalen
Jackson Robert W
Selengut Jeremy
Dodson Robert
Brinkac Lauren M
Daugherty Sean C
Deboy Robert
Durkin A Scott
Giglio Michelle Gwinn
Madupu Ramana
Nelson William C
Rosovitz M J
Sullivan Steven
Crabtree Jonathan
Creasy Todd
Davidsen Tanja
Haft Dan H
Zafar Nikhat
Zhou Liwei
Halpin Rebecca
Holley Tara
Khouri Hoda
Feldblyum Tamara
White Owen
Fraser Claire M
Chatterjee Arun K
Cartinhour Sam
Schneider David J
Mansfield John
Collmer Alan
Buell C Robin
References (68)
68 references, click to expand
  1. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7.
    Nature. 2001 Jan 25;409(6819):529-33 PMID: 11206551
  2. Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains.
    Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12403-8 PMID: 12205291
  3. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440.
    Environ Microbiol. 2002 Dec;4(12):799-808 PMID: 12534463
  4. 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.
    Mol Microbiol. 1998 Jul;29(1):165-77 PMID: 9701811
  5. Analysis of the argK-tox gene cluster in nontoxigenic strains of Pseudomonas syringae pv. phaseolicola.
    Appl Environ Microbiol. 2003 Aug;69(8):4979-82 PMID: 12902295
  6. 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.
    Appl Environ Microbiol. 2005 Jul;71(7):3778-85 PMID: 16000789
  7. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities.
    Nature. 2002 May 23;417(6887):459-63 PMID: 12024217
  8. Isolation and characterization of a second exe operon required for extracellular protein secretion in Aeromonas hydrophila.
    J Bacteriol. 1994 Nov;176(22):6819-26 PMID: 7961440
  9. Comparison of Ethylene Production by Pseudomonas syringae and Ralstonia solanacearum.
    Phytopathology. 1999 May;89(5):360-5 PMID: 18944747
  10. Type III secretion system effector proteins: double agents in bacterial disease and plant defense.
    Annu Rev Phytopathol. 2004;42:385-414 PMID: 15283671
  11. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13979-84 PMID: 11087840
  12. Characterization of genes required for pilus expression in Pseudomonas syringae pathovar phaseolicola.
    J Bacteriol. 1996 Jan;178(2):410-7 PMID: 8550460
  13. Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5.
    Nat Biotechnol. 2005 Jul;23(7):873-8 PMID: 15980861
  14. Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity.
    Curr Opin Plant Biol. 2004 Aug;7(4):384-90 PMID: 15231260
  15. Comparative genomic analysis of plant-associated bacteria.
    Annu Rev Phytopathol. 2002;40:169-89 PMID: 12147758
  16. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen.
    Nature. 2000 Aug 31;406(6799):959-64 PMID: 10984043
  17. Molecular cloning in Escherichia coli, expression, and nucleotide sequence of the gene for the ethylene-forming enzyme of Pseudomonas syringae pv. phaseolicola PK2.
    Biochem Biophys Res Commun. 1992 Oct 30;188(2):826-32 PMID: 1445325
  18. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor.
    Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):2275-80 PMID: 11854524
  19. The HopPtoF locus of Pseudomonas syringae pv. tomato DC3000 encodes a type III chaperone and a cognate effector.
    Mol Plant Microbe Interact. 2004 May;17(5):447-55 PMID: 15141948
  20. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):266-92 PMID: 10357851
  21. Isolation and characterization of the gene from Pseudomonas syringae pv. phaseolicola encoding the phaseolotoxin-insensitive ornithine carbamoyltransferase.
    Mol Gen Genet. 1990 Jul;222(2-3):461-6 PMID: 2274044
  22. Structure and evolution of plant disease resistance genes.
    J Appl Genet. 2002;43(4):403-14 PMID: 12441626
  23. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen.
    Appl Environ Microbiol. 2004 Apr;70(4):1999-2012 PMID: 15066790
  24. The AprX protein of Pseudomonas aeruginosa: a new substrate for the Apr type I secretion system.
    Gene. 2001 Jan 10;262(1-2):147-53 PMID: 11179678
  25. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae.
    Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2549-54 PMID: 15701698
  26. Functions of the gene products of Escherichia coli.
    Microbiol Rev. 1993 Dec;57(4):862-952 PMID: 7508076
  27. Lineage-specific regions in Pseudomonas syringae pv tomato DC3000.
    Mol Plant Pathol. 2005 Jan 1;6(1):53-64 PMID: 20565638
  28. Genome sequence of the plant pathogen Ralstonia solanacearum.
    Nature. 2002 Jan 31;415(6871):497-502 PMID: 11823852
  29. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis.
    Cell. 2002 May 31;109(5):575-88 PMID: 12062101
  30. A novel type II secretion system in Pseudomonas aeruginosa.
    Mol Microbiol. 2002 Jan;43(2):475-85 PMID: 11985723
  31. The TIGRFAMs database of protein families.
    Nucleic Acids Res. 2003 Jan 1;31(1):371-3 PMID: 12520025
  32. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte.
    Microbiol Mol Biol Rev. 2000 Sep;64(3):624-53 PMID: 10974129
  33. A whole-genome assembly of Drosophila.
    Science. 2000 Mar 24;287(5461):2196-204 PMID: 10731133
  34. The versatile bacterial type IV secretion systems.
    Nat Rev Microbiol. 2003 Nov;1(2):137-49 PMID: 15035043
  35. Control of ethylene synthesis by expression of a bacterial enzyme in transgenic tomato plants.
    Plant Cell. 1991 Nov;3(11):1187-93 PMID: 1821764
  36. Improved microbial gene identification with GLIMMER.
    Nucleic Acids Res. 1999 Dec 1;27(23):4636-41 PMID: 10556321
  37. Map-based cloning of a protein kinase gene conferring disease resistance in tomato.
    Science. 1993 Nov 26;262(5138):1432-6 PMID: 7902614
  38. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants.
    J Bacteriol. 1986 Nov;168(2):512-22 PMID: 3023280
  39. 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.
    Proc Natl Acad Sci U S A. 1999 Sep 14;96(19):10875-80 PMID: 10485919
  40. Type IV transporters of pathogenic bacteria.
    Curr Opin Microbiol. 2003 Feb;6(1):29-34 PMID: 12615216
  41. Genes encoding a cellulosic polymer contribute toward the ecological success of Pseudomonas fluorescens SBW25 on plant surfaces.
    Mol Ecol. 2003 Nov;12(11):3109-21 PMID: 14629390
  42. Molecular, functional, and evolutionary analysis of sequences specific to Salmonella.
    Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1033-7 PMID: 8430070
  43. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter.
    J Bacteriol. 2004 Jan;186(2):543-55 PMID: 14702323
  44. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000.
    Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10181-6 PMID: 12928499
  45. Nucleotide sequence and evolution of the five-plasmid complement of the phytopathogen Pseudomonas syringae pv. maculicola ES4326.
    J Bacteriol. 2004 Aug;186(15):5101-15 PMID: 15262947
  46. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease.
    EMBO J. 2000 Jul 3;19(13):3204-14 PMID: 10880434
  47. Phylogeny of the replication regions of pPT23A-like plasmids from Pseudomonas syringae.
    Microbiology. 2000 Oct;146 ( Pt 10):2375-84 PMID: 11021914
  48. The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum.
    Planta. 2001 Jun;213(2):241-9 PMID: 11469589
  49. Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae.
    Mol Plant Microbe Interact. 2004 May;17(5):521-31 PMID: 15141956
  50. Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae.
    Mol Plant Microbe Interact. 2005 Apr;18(4):275-82 PMID: 15828679
  51. Complete genome sequence of Caulobacter crescentus.
    Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):4136-41 PMID: 11259647
  52. Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease.
    Mol Microbiol. 1999 Aug;33(3):612-22 PMID: 10417651
  53. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells.
    Curr Opin Microbiol. 2003 Feb;6(1):20-8 PMID: 12615215
  54. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  55. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean.
    Plant Cell. 1991 Jan;3(1):49-59 PMID: 1824334
  56. Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster.
    J Mol Evol. 1999 Nov;49(5):627-44 PMID: 10552044
  57. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria.
    Curr Opin Microbiol. 2004 Feb;7(1):11-8 PMID: 15036134
  58. Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose.
    Mol Microbiol. 2003 Oct;50(1):15-27 PMID: 14507360
  59. Characterization of the alginate biosynthetic gene cluster in Pseudomonas syringae pv. syringae.
    J Bacteriol. 1997 Jul;179(14):4464-72 PMID: 9226254
  60. Comparative genomic analysis of the pPT23A plasmid family of Pseudomonas syringae.
    J Bacteriol. 2005 Mar;187(6):2113-26 PMID: 15743960
  61. Genome Properties: a system for the investigation of prokaryotic genetic content for microbiology, genome annotation and comparative genomics.
    Bioinformatics. 2005 Feb 1;21(3):293-306 PMID: 15347579
  62. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  63. IS801, an insertion sequence element isolated from Pseudomonas syringae pathovar phaseolicola.
    Mol Microbiol. 1991 Mar;5(3):617-22 PMID: 1646375
  64. Gene-for-gene complementarity in plant-pathogen interactions.
    Annu Rev Genet. 1990;24:447-63 PMID: 2088175
  65. Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition.
    Curr Opin Microbiol. 2002 Feb;5(1):44-50 PMID: 11834368
  66. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  67. Assembly and function of type III secretory systems.
    Annu Rev Microbiol. 2000;54:735-74 PMID: 11018143
  68. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death.
    J Bacteriol. 1997 Sep;179(18):5655-62 PMID: 9294418
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.187.18.6488-6498.2005
Published
2005-09-00
Pages
6488-98
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1236638
Subset
IM
External Links
PubMed source DOI: 10.1128/JB.187.18.6488-6498.2005 PMC Full Text View journal details
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