Phylogenetic position and virulence apparatus of the pear flower necrosis pathogen Erwinia piriflorinigrans CFBP 5888T as assessed by comparative genomics

Systematic and Applied Microbiology

Volumn 36, Issue 7, 2013, Pages 449-456

  Smits, Theo H M ^a   Rezzonico, Fabio ^a   López, María M ^b   Blom, Jochen ^c   Goesmann, Alexander ^c   Frey, Jürg E ^a   Duffy, Brion ^a  

^a AGROSCOPE   (Switzerland)

^b INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^c BIELEFELD UNIVERSITY   (Germany)

Author keywords

Bacterial evolution; Fire blight; Pathoadaptation; Phylogeny; Rosaceae; Virulence

Indexed keywords

CHRYSOBACTIN; DEFEROXAMINE; SIDEROPHORE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENOME; BACTERIAL SOFT ROT; BACTERIAL VIRULENCE; BIOSYNTHESIS; EPIPHYTE; ERWINIA; ERWINIA AMYLOVORA; ERWINIA PIRIFLORINIGRANS CFBP 5888; ERWINIA PYRIFOLIAE; ERWINIA TASMANIENSIS; FIRE BLIGHT; FLOWER; GENE SEQUENCE; GENE TRANSFER; GENOME SIZE; GENUS; NECROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMS BY PHYLOGENETIC POSITION; PEAR; PECTOBACTERIUM; PRIORITY JOURNAL; TANDEM REPEAT; TYPE III SECRETION SYSTEM; TYPE STRAIN; TYPE VI SECRETION SYSTEM;

BACTERIA (MICROORGANISMS); DICKEYA; ERWINIA; ERWINIA AMYLOVORA; ERWINIA PYRIFOLIAE; PECTOBACTERIUM; PYRUS; PYRUS PYRIFOLIA VAR. CULTA; ROSACEAE;

BACTERIAL EVOLUTION; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR; CRISPR REPEAT REGION; CRR; EPS; EXOPOLYSACCHARIDE; FIRE BLIGHT; ICE; INTEGRATIVE CONJUGATIVE ELEMENT; NON-RIBOSOMAL PEPTIDE SYNTHASES/POLYKETIDE SYNTHASES; NRPS/PKS; PATHOADAPTATION; PHYLOGENY; ROSACEAE; T1SS; T2SS; T3SS; T6SS; TYPE I SECRETION SYSTEM; TYPE II SECRETION SYSTEM; TYPE III SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; VIRULENCE;

BASE SEQUENCE; CLUSTER ANALYSIS; DNA, BACTERIAL; ERWINIA; FLOWERS; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLASMIDS; PYRUS; SEQUENCE ANALYSIS, DNA; SPAIN; VIRULENCE FACTORS;

EID: 84884206544     PISSN: 07232020     EISSN: 16180984     Source Type: Journal    
DOI: 10.1016/j.syapm.2013.04.003     Document Type: Article

References (65)

1. Badger J.H., Olsen G.J. CRITICA: coding region identification tool invoking comparative analysis. Mol. Biol. Evol. 1999, 16:512-524.
2. Barbé S., Llop P., Blom J., Cabrefiga J., Goesmann A., Duffy B., Montesinos E., Smits T.H.M., López M.M. Complete sequence of Erwinia piriflorinigrans plasmids pEPIR37 and pEPIR5 and role of pEPIR37 in pathogen virulence. Plant Pathol. 2012, 10.1111/ppa.12002.
3. Barnes H.H., Ishimaru C.A. Purification of catechol siderophores by boronate affinity chromatography: identification of chrysobactin from Erwinia carotovora subsp. carotovora. BioMetals 1999, 12:83-87.
4. Beer S.V., Kim J.-H., Zumoff C.H., Bogdanove A.J., Laby R.J., Tanii A., Tamura O., Gustafson H.L., Momol T., Aldwinckle H.S. Characterization of bacteria that cause bacterial shoot blight of pear in Japan. Acta Hort. 1996, 411:179-181.
5. Bernhard F., Coplin D., Geider K. A gene cluster for amylovoran synthesis in Erwinia amylovora: characterization and relationship to cps gene in Erwinia stewartii. Mol. Gen. Genet. 1993, 239:158-168.
6. Blom J., Albaum S.P., Doppmeier D., Pühler A., Vorhölter F.-J., Zakrzewski M., Goesmann A. EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 2009, 10:154.
7. Bonn W.G., van der Zwet T. Distribution and economic importance of fire blight. Fire blight: the disease and its causative agent, Erwinia amylovora 2000, 37-53. CAB, International, Wallingford, UK. J.L. Vanneste (Ed.).
8. Brady C.L., Cleenwerck I., Denman S., Venter S.N., Rodríguez-Palenzuela P., Coutinho T.A., De Vos P. Proposal to reclassify Brenneria quercina (Hildebrand & Schroth 1967) Hauben et al. 1999 into a novel genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov. and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. Int. J. Syst. Evol. Microbiol. 2012, 62:1592-1602.
9. Brouns S.J.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J.H., Snijders A.P.L., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J. Small CRISPR RNAs guide antiviral defence in prokaryotes. Science 2008, 321:960-964.
10. Coplin D.L., Majerczak D.R., Bugert P., Geider K. Nucleotide sequence analysis of the Erwinia stewartii cps gene cluster for synthesis of stewartan and comparison to the Erwinia amylovora ams cluster for synthesis of amylovoran. Acta Hort. 1996, 411:251-257.
11. Darling A.E., Treangen T.J., Messeguer X., Perna N.T. Analyzing patterns of microbial evolution using the Mauve genome alignment system. Methods Mol. Biol. 2008, 396:135-152.
12. Davis L.G., Dibner M.D., Battley J.F. Basic Methods in Molecular Biology 1990, Elsevier, New York, NY.
13. de la Cruz F., Frost L.S., Meyer R.J., Zechner E.L. Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol. Rev. 2010, 34:18-40.
14. De Maayer P., Venter S.N., Kamber T., Duffy B., Coutinho T.A., Smits T.H.M. Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 2011, 12:576.
15. Duffy B., Schärer H.-J., Bünter M., Klay A., Holliger E. Regulatory measures against Erwinia amylovora in Switzerland. EPPO Bull. 2005, 35:239-244.
16. Expert D. Withholding and exchanging iron: interactions between Erwinia spp. and their host plants. Annu. Rev. Phytopathol. 1999, 37:307-334.
17. Feistner G.J., Stahl D.C., Gabrik A.H. Proferrioxamine siderophores of Erwinia amylovora. A capillary liquid chromatographic/electrospray tandem mass spectrometry study. Org. Mass Spectrom. 1993, 28:163-175.
18. Franza T., Enard C., van Gijsegem F., Expert D. Genetic analysis of the Erwinia chrysanthemi 3937 chrysobactin iron-transport system: characterization of a gene cluster involved in uptake and biosynthetic pathways. Mol. Microbiol. 1991, 5:1319-1329.
19. Geider K., Auling G., Jakovljevic V., Völksch B. A polyphasic approach assigns the pathogenic Erwinia strains from diseased pear trees in Japan to Erwinia pyrifoliae. Lett. Appl. Microbiol. 2009, 48:324-330.
20. Gross M., Geier G., Rudolph K., Geider K. Levan and levansucrase synthesized by the fireblight pathogen Erwinia amylovora. Physiol. Mol. Plant Pathol. 1992, 40:371-381.
21. Guglielmini J., Quintais L., Garcillán-Barcia M.P., de la Cruz F., Rocha E.P.C. The repertoire of ICE in prokaryotes underscores the unity, diversity and ubiquity of conjugation. PLoS Genet 2011, 7:e1002222.
22. Hauben L., Swings J. Genus XIII. Erwinia. The Proteobacteria, Part B: the Gammaproteobacteria 2005, vol. 2:670-679. Springer, New York. 2nd ed. D.J. Brenner, N.R. Krieg, J.T. Staley, G.M. Garrity (Eds.).
23. Kamber T., Smits T.H.M., Rezzonico F., Duffy B. Genomics and current genetic understanding of Erwinia amylovora and the fire blight antagonist Pantoea vagans. Trees Struct. Funct. 2012, 26:227-238.
24. Kanehisa M., Goto S., Kawashima S., Nakaya A. The KEGG databases at GenomeNet. Nucleic Acids Res. 2002, 30:42-46.
25. Kim W.-S., Gardan L., Rhim S.-L., Geider K. Erwinia pyrifoliae sp. nov., a novel pathogen that affects Asian pear trees (Pyrus pyrifolia Nakai). Int. J. Syst. Bacteriol. 1999, 49:899-906.
26. Kim W.-S., Hildebrand M., Jock S., Geider K. Molecular comparison of pathogenic bacteria from pear trees in Japan and the fire blight pathogen Erwinia amylovora. Microbiology 2001, 147:2951-2959.
27. Konstantinidis K.T., Tiedje J.M. Towards a genome-based taxonomy for prokaryotes. J. Bacteriol. 2005, 187:6258-6264.
28. Kube M., Migdoll A.M., Gehring I., Heitmann K., Mayer Y., Kuhl H., Knaust F., Geider K., Reinhardt R. Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genomics 2010, 11:393.
29. Kube M., Migdoll A.M., Müller I., Kuhl H., Beck A., Reinhardt R., Geider K. The genome of Erwinia tasmaniensis strain Et1/99, a non-pathogenic bacterium in the genus Erwinia. Environ. Microbiol. 2008, 10:2211-2222.
30. Llop P., Barbé S., López M.M. Functions and origin of plasmids in Erwinia species that are pathogenic to or epiphytically associated with pome fruit trees. Trees Struct. Funct. 2012, 26:31-46.
31. López M.M., Roselló M., Llop P., Ferrer S., Christen R., Gardan L. Erwinia piriflorinigrans sp. nov., a novel pathogen that causes necrosis of pear blossoms. Int. J. Syst. Evol. Microbiol. 2011, 61:561-567.
32. Malnoy M., Martens S., Norelli J.L., Barny M.-A., Sundin G.W., Smits T.H.M., Duffy B. Fire blight: applied genomic insights of the pathogen and the host. Annu. Rev. Phytopathol. 2012, 50:475-494.
33. Mann R.A., Blom J., Bühlmann A., Plummer K.M., Beer S.V., Luck J.E., Goesmann A., Frey J.E., Rodoni B.C., Duffy B., Smits T.H.M. Comparative analysis of the Hrp pathogenicity island of Rubus- and Spiraeoideae-infecting Erwinia amylovora strains identifies the IT region as a remnant of an integrative conjugative element. Gene 2012, 504:6-12.
34. Mann R.A., Smits T.H.M., Bühlmann A., Blom J., Goesmann A., Frey J.E., Plummer K.M., Beer S.V., Luck J., Duffy B., Rodoni B. Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS One 2013, 8:e55644.
35. Matsuura T., Mizuno A., Tsukamoto T., Shimizu Y., Saito N., Sato S., Kikuchi S., Uzuki T., Azegami K., Sawada H. Erwinia uzenensis sp. nov., a novel pathogen that affects European pear trees (Pyrus communis L.). Int. J. Syst. Evol. Microbiol. 2012, 62:1799-1803.
36. Matsuura T., Shinohara H., Inoue Y., Azegami K., Tsushima S., Tsukamoto T., Mizuno A. Erwinia isolates from the bacterial shoot blight of pear in Japan are closely related to Erwinia pyrifoliae based on phylogenetic analyses of gyrB and rpoD genes. J. Gen. Plant Pathol. 2007, 73:53-58.
37. McGhee G.C., Sundin G.W. Erwinia amylovora CRISPR elements provide new tools for evaluating strain diversity and for microbial source tracking. PLoS One 2012, 7:e41706.
38. McHardy A.C., Goesmann A., Pühler A., Meyer F. Development of joint application strategies for two microbial gene finders. Bioinformatics 2004, 20:1622-1631.
39. Medema M.H., Blin K., Cimermancic P., de Jager V., Zakrzewski P., Fischbach M.A., Weber T., Takano E., Breitling R. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res. 2011, 39:W339-W346.
40. Meyer F., Goesmann A., McHardy A.C., Bartels D., Bekel T., Clausen J., Kalinowski J., Linke B., Rupp O., Giegerich R., Pühler A. GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 2003, 31:2187-2195.
41. Mizuno A., Sato S., Kawai A., Nishiyama K. Taxonomic position of the causal pathogen of bacterial shoot blight of pear. J. Gen. Plant Pathol. 2000, 66:48-58.
42. Mizuno A., Tsukamoto T., Shimizu Y., Ooya H., Matsuura T., Saito N., Sato S., Kikuchi S., Uzuki T., Azegami K. Occurrence of bacterial black shoot disease of European pear in Yamagata prefecture. J. Gen. Plant Pathol. 2010, 76:43-51.
43. Mohammadi M., Geider K. Autoinducer-2 of the fire blight pathogen Erwinia amylovora and other plant-associated bacteria. FEMS Microbiol. Lett. 2007, 266:34-41.
44. Molina L., Rezzonico F., Défago G., Duffy B. Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J. Bacteriol. 2005, 187:3206-3213.
45. Moretti C., Hosni T., Vandemeulebroecke K., Brady C., De Vos P., Buonaurio R., Cleenwerck I. Erwinia oleae sp. nov., isolated from olive knots caused by Pseudomonas savastanoi pv. savastanoi. Int. J. Syst. Evol. Microbiol. 2011, 61:2745-2752.
46. Müller I., Lurz R., Geider K. Tasmancin and lysogenic bacteriophages induced from Erwinia tasmaniensis strains. Microbiol. Res. 2012, 167:381-387.
47. Oh C.-S., Beer S.V. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol. Lett. 2005, 253:185-192.
48. Oh C.-S., Kim J.F., Beer S.V. The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infection. Mol. Plant Pathol. 2005, 6:125-138.
49. Palacio-Bielsa A., Roselló M., Llop P., López M.M. Erwinia spp. from pome fruit trees: similarities and differences among pathogenic and non-pathogenic species. Trees Struct. Funct. 2012, 26:13-29.
50. Park D.H., Thapa S.P., Choi B.-S., Kim W.-S., Hur J.H., Cho J.M., Lim J.-S., Choi I.-Y., Lim C.K. Complete genome sequence of Japanese Erwinia strain Ejp617, a bacterial shoot blight pathogen of pear. J. Bacteriol. 2011, 193:586-587.
51. Paszkiewicz K., Studholme D.J. De novo assembly of short sequence reads. Brief Bioinformatics 2010, 11:457-472.
52. Pourcel C., Salvignol F., Vergnaud G. CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. Microbiology 2005, 151:653-663.
53. Powney R., Smits T.H.M., Sawbridge T., Frey B., Blom J., Frey J.E., Plummer K.M., Beer S.V., Luck J., Duffy B., Rodoni B. Genome sequence of an Erwinia amylovora strain with restricted pathogenicity to Rubus plants. J. Bacteriol. 2011, 193:785-786.
54. Rezzonico F., Smits T.H.M., Duffy B. Diversity, evolution and functionality of clustered regularly interspaced short palindromic repeat (CRISPR) regions in fire blight pathogen Erwinia amylovora. Appl. Environ. Microbiol. 2011, 77:3819-3829.
55. Roselló M., Peñalver J., Llop P., Gorris M.T., Chartier R., García F., Montón C., Cambra M., López M.M. Identification of an Erwinia sp. different from Erwinia amylovora and responsible for necrosis on pear blossoms. Can. J. Plant Pathol. 2006, 28:30-41.
56. Saier M.H., Yen M.R., Noto K., Tamang D.G., Elkan C. The transporter classification database: recent advances. Nucleic Acids Res. 2009, 37:D274-D278.
57. Salzberg S.L., Delcher A.L., Kasif S., White O. Microbial gene identification using interpolated Markov models. Nucleic Acids Res. 1998, 26:544-548.
58. Smits T.H.M., Duffy B. Genomics of iron-acquisition in the plant pathogen Erwinia amylovora: insights in the biosynthetic pathway of the siderophore desferrioxamine E. Arch. Microbiol. 2011, 193:693-699.
59. T and comparative genomic insights into plant pathogenicity. BMC Genomics 2010, 11:2.
60. Smits T.H.M., Rezzonico F., Duffy B. Evolutionary insights from Erwinia amylovora genomics. J. Biotechnol. 2011, 155:34-39.
61. Smits T.H.M., Rezzonico F., Kamber T., Blom J., Goesmann A., Frey J.E., Duffy B. Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp. Mol. Plant-Microbe. Interact. 2010, 23:384-393.
62. Sorek R., Kunin V., Hugenholtz P. CRISPR - a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat. Rev. Microbiol. 2008, 6:181-186.
63. Venturi V., Venuti C., Devescovi G., Lucchese C., Friscina A., Degrassi G., Aguilar C., Mazzucchi U. The plant pathogen Erwinia amylovora produces acyl-homoserine lactone signal molecules in vitro and in planta. FEMS Microbiol. Lett. 2004, 241:179-183.
64. Wang D., Korban S.S., Zhao Y. The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. Mol. Plant Pathol. 2009, 10:277-290.
65. Zhao Y., Sundin G.W., Wang D. Construction and analysis of pathogenicity island deletion mutants of Erwinia amylovora. Can. J. Microbiol. 2009, 55:457-464.