Complete genome sequence of the fire blight pathogen Erwinia pyrifoliae DSM 12163T and comparative genomic insights into plant pathogenicity

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Smits, Theo H M ^a   Jaenicke, Sebastian ^b   Rezzonico, Fabio ^a   Kamber, Tim ^a   Goesmann, Alexander ^b   Frey, Jürg E ^a   Duffy, Brion ^a  

^a AGROSCOPE   (Switzerland)

^b BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SORBITOL; TRANSPOSASE; VIRULENCE FACTOR; BACTERIAL DNA;

ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL VIRULENCE; CONTROLLED STUDY; EPIPHYTE; ERWINIA; ERWINIA PYRIFOLIAE; ERWINIA TASMANIENSIS; FIRE BLIGHT; GENE DELETION; GENE SEQUENCE; GENOMIC ISLAND; HOST RANGE; IRON TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POME FRUIT; PYROSEQUENCING; QUORUM SENSING; TYPE III SECRETION SYSTEM; TYPE STRAIN; COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTER PROGRAM; DNA SEQUENCE; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY; PLANT DISEASE;

ERWINIA; ERWINIA AMYLOVORA; ERWINIA PYRIFOLIAE; PYRUS PYRIFOLIA VAR. CULTA;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; ERWINIA; GENOME, BACTERIAL; GENOMIC ISLANDS; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLASMIDS; SEQUENCE ANALYSIS, DNA; SOFTWARE; VIRULENCE FACTORS;

EID: 77249161812     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-2     Document Type: Article

References (82)

1. Duffy B, Schärer H-J, Bünter M, Klay A, Holliger E. Regulatory measures against Erwinia amylovora in Switzerland. EPPO Bull 2005, 35:239-244.
2. Bonn WG, Zwet T. Distribution and economic importance of fire blight. Fire blight the disease and its causative agent, Erwinia amylovora 2000, 37-53. Wallingford, UK CAB International, Vanneste JL.
3. Jock S, Donat V, López MM, Bazzi C, Geider K. Following spread of fire blight in Western, Central and Southern Europe by molecular differentiation of Erwinia amylovora strains with PFGE analysis. Environ Microbiol 2002, 4(2):106-114. 10.1046/j.1462-2920.2002.00277.x, 11972620.
4. Thomson SV. Epidemiology of fire blight. Fire blight the disease and its causative agent, Erwinia amylovora 2000, 9-36. Wallingford, UK CAB International, Vanneste JL.
5. Johnson KB, Stockwell VO. Management of fire blight a case study in microbial ecology. Annu Rev Phytopathol 1998, 36:227-248. 10.1146/annurev.phyto.36.1.227, 15012499.
6. 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. 10.1111/j.1472-765X.2008.02535.x, 19187512.
7. 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.
8. McGhee GC, Schnabel EL, Maxson-Stein K, Jones B, Stromberg VK, Lacy GH, Jones AL. Relatedness of chromosomal and plasmid DNAs of Erwinia pyrifoliae and Erwinia amylovora. Appl Environ Microbiol 2002, 68(12):6182-6192. 10.1128/AEM.68.12.6182-6192.2002, 134437, 12450843.
9. 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.
10. Lehman SM, Kim W-S, Castle AJ, Svircev AM. Duplex real-time polymerase chain reaction reveals competition between Erwinia amylovora and E. pyrifoliae on pear blossoms. Phytopathology 2008, 98(6):673-679. 10.1094/PHYTO-98-6-0673, 18944291.
11. Eastgate JA. Erwinia amylovora the molecular basis of fireblight disease. Mol Plant Pathol 2000, 1(6):325-329.
12. Oh C-S, Beer SV. Molecular genetics of Erwinia amylovora involved in the development of fire blight. FEMS Microbiol Lett 2005, 253:185-192. 10.1016/j.femsle.2005.09.051, 16253442.
13. Triplett LR, Zhao Y, Sundin GW. Genetic differences between blight-causing Erwinia species with differing host specificities, identified by suppression subtractive hybridization. Appl Environ Microbiol 2006, 72(11):7359-7364. 10.1128/AEM.01159-06, 1636173, 16963554.
14. Shrestha R, Lee SH, Kim JE, Wilson C, Choi S-G, Park DH, Wang MH, Hur JH, Lim CK. Diversity and detection of Korean Erwinia pyrifoliae strains as determined by plasmid profiling, phylogenetic analysis and PCR. Plant Pathol 2007, 56:1023-1031.
15. Shrestha R, Tsuchiya K, Baek SJ, Bae HN, Hwang I, Hur JH, Lim CK. Identification of dspEF, hrpW and hrpN loci and characterization of the hrpNEp gene in Erwinia pyrifoliae. J Gen Plant Pathol 2005, 71:211-220.
16. Kube M, Migdoll AM, 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(9):2211-2222. 10.1111/j.1462-2920.2008.01639.x, 18462403.
17. Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, et al. GenDB - an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 2003, 31:2187-2195. 10.1093/nar/gkg312, 153740, 12682369.
18. Maxson-Stein K, McGhee GC, Smith JJ, Jones AL, Sundin GW. Genetic analysis of a pathogenic Erwinia sp. isolated from pear in Japan. Phytopathology 2003, 93(11):1393-1399. 10.1094/PHYTO.2003.93.11.1393, 18944067.
19. Rhim S-L, Völksch B, Gardan L, Paulin J-P, Langlotz C, Kim W-S, Geider K. Erwinia pyrifoliae an Erwinia species different from Erwinia amylovora causes a necrotic disease of Asian pear trees. Plant Pathol 1999, 48:514-520.
20. Fu J-F, Chang H-C, Chen Y-M, Chang Y-S, Liu S-T. Sequence analysis of an Erwinia stewartii plasmid, pSW100. Plasmid 1995, 34(2):75-84. 10.1006/plas.1995.9999, 8559805.
21. Lonetto M, Gribskov M, Gross CA. The s70 family sequence conservation and evolutionary relationships. J Bacteriol 1992, 174(12):3843-3849. 206090, 1597408.
22. Anderson M, Pollitt CE, Roberts IS, Eastgate JA. Identification and characterization of the Erwinia amylovora rpoS gene RpoS is not involved in induction of fireblight disease symptoms. J Bacteriol 1998, 180:6789-6792. 107793, 9852034.
23. Andersson RA, Kõiv V, Norman-Setterblad C, Pirhonen M. Role of RpoS in virulence and stress tolerance of the plant pathogen Erwinia carotovora subsp. carotovora. Microbiology 1999, 145:3547-3556.
24. Mukherjee A, Cui Y, Ma W, Liu Y, Ishihama A, Eisenstark A, Chatterjee AK. RpoS (Sigma-S) controls expression of rsmAa global regulator of secondary metabolites, harpin and extracellular proteins in Erwinia carotovora. J Bacteriol 1998, 180:3629-3634. 107332, 9658007.
25. Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 1998, 62(2):379-433. 98920, 9618447.
26. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X. Molecular basis of symbiosis between Rhizobium and legumes. Nature 1997, 387:394-401. 10.1038/387394a0, 9163424.
27. Göttfert M, Röthlisberger S, Kündig C, Beck C, Marty R, Hennecke H. Potential symbiosis-specific genes uncovered by sequencing a 410-kilobase DNA region of the Bradyrhizobium japonicum chromosome. J Bacteriol 2001, 183(4):1405-1412. 10.1128/JB.183.4.1405-1412.2001, 95015, 11157954.
28. Dale C, Young SA, Haydon DT, Welburn SC. The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci USA 2001, 98(4):1883-1888. 10.1073/pnas.021450998, 29351, 11172045.
29. Alfano JR, Collmer A. Type III secretion system effector proteins double agents in bacterial disease and plant defence. Annu Rev Phytopathol 2004, 42:385-414. 10.1146/annurev.phyto.42.040103.110731, 15283671.
30. Jock S, Kim W-S, Barny M-A, Geider K. Molecular characterization of natural Erwinia pyrifoliae strains deficient in hypersensitive response. Appl Environ Microbiol 2003, 69(1):679-682. 10.1128/AEM.69.1.679-682.2003, 152409, 12514060.
31. McClelland M, Sanderson KE, Spieth J, Clifton SW, Latreille P, Courtney L, Porwollik S, Ali J, Dante M, Du F, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001, 413:852-856. 10.1038/35101614, 11677609.
32. Oh C-S, Kim JF, Beer SV. The Hrp pathogenicity island of Erwinia amylovora and identification of three novel genes required for systemic infection. Mol Plant Pathol 2005, 6(2):125-138.
33. Shrestha R, Lee SH, Cho S, Lim CK, Hong S, Cho JM, Hwang I, Hur JH, Kim W-S. The hrp genes cluster in Erwinia pyrifoliae and determination of HR active domain in HrpNEp protein. Acta Hort 2008, 793:221-230.
34. Boureau T, ElMaarouf-Bouteau H, Garnier A, Brisset M-N, Perino C, Pucheu I, Barny M-A. DspA/E, a type III effector essential for Erwinia amylovora pathogenicity and growth in planta, induces cell death in host apple and nonhost tobacco plants. Mol Plant-Microbe Interact 2006, 19(1):16-24. 10.1094/MPMI-19-0016, 16404949.
35. Petnicki-Ocwieja T, van Dijk K, Alfano JR. The hrpK operon of Pseudomonas syringae pv. tomato DC3000 encodes two proteins secreted by the type III (Hrp) protein secretion system HopB1 and HrpK, a putative type III translocator. J Bacteriol 2005, 187(2):649-663. 10.1128/JB.187.2.649-663.2005, 543549, 15629936.
36. Bocsanczy AM, Beer SV, Perna NT, Biehl B, Glasner JD, Cartinhour SW, Schneider DJ, DeClerck GA, Sebaihia M, Parkhill J, et al. Contributions of the genome sequence of Erwinia amylovora to the fire blight community. Acta Hort 2008, 793:163-170.
37. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis what can be learnt from available microbial genomic resources?. BMC Genomics 2009, 10:104. 10.1186/1471-2164-10-104, 2660368, 19284603.
38. Bingle LEH, Bailey CM, Pallen MJ. Type VI secretion a beginner's guide. Curr Opin Microbiol 2008, 11(1):3-8. 10.1016/j.mib.2008.01.006, 18289922.
39. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 2006, 103(5):1528-1533. 10.1073/pnas.0510322103, 1345711,1345711, 16432199.
40. Mattinen L, Nissinen R, Riipi T, Kalkkinen N, Pirhonen M. Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 2007, 7:3527-3537. 10.1002/pmic.200600759, 17726675.
41. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, Humphris S, Burr T, Takle G, Brurberg M-B, Birch PRJ, et al. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 2008, 4(6):e1000093. 10.1371/journal.ppat.1000093, 2413422, 18566662.
42. Roest HP, Mulders IHM, Spaink HP, Wijffelman CA, Lugtenberg BJJ. A Rhizobium leguminosarum biovar trifolii locus not localized on the Sym plasmid hinders effective nodulation on plants of the pea cross-inoculation group. Mol Plant-Microbe Interact 1997, 10(7):938-941. 10.1094/MPMI.1997.10.7.938, 9304865.
43. Bell KS, Sebaihia M, Pritchard L, Holden MTG, Hyman LJ, Holeva MC, Thomson NR, Bentley SD, Churcher LJC, Mungall K. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 2004, 101(30):11105-11110. 10.1073/pnas.0402424101, 503747, 15263089.
44. Aldridge P, Metzger M, Geider K. Genetics of sorbitol metabolism in Erwinia amylovora and its influence on bacterial virulence. Mol Gen Genet 1997, 256(6):611-619. 10.1007/s004380050609, 9435786.
45. Teo G, Suzuki Y, Uratsu SL, Lampinen B, Ormonde N, Hu WK, DeJong TM, Dandekar AM. Silencing leaf sorbitol synthesis alters long-distance partitioning and apple fruit quality. Proc Natl Acad Sci USA 2006, 103(49):18842-18847. 10.1073/pnas.0605873103, 1693749, 17132742.
46. Duffy B, Dandekar AM. Sorbitol has no role in fire blight as demonstrated using transgenic apple with constitutively altered content. Acta Hort 2008, 793:279-283.
47. Suleman P, Steiner PW. Relationship between sorbitol and solute potential in apple shoots relative to fire blight symptom development after infection by Erwinia amylovora. Phytopathology 1994, 84:1244-1250.
48. Kim W-S, Schollmeyer M, Nimtz M, Wray V, Geider K. Genetics of biosynthesis and structure of the capsular exopolysaccharide from the Asian pear pathogen Erwinia pyrifoliae. Microbiology 2002, 148:4015-4024.
49. Bernhard F, Schullerus D, Bellemann P, Geider K, Nimtz M, Majerczak DR, Coplin DL. Genetics and complementation of DNA regions involved in amylovoran synthesis of Erwinia amylovora and stewartan synthesis of Erwinia stewartii. Acta Hort 1996, 411:269-274.
50. Coplin DL, Majerczak DR, 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.
51. Gross M, Geier G, Rudolph K, Geider K. Levan and levansucrase synthesized by the fireblight pathogen Erwinia amylovora. Physiol Mol Plant Pathol 1992, 40(6):371-381.
52. Pierson LS, Wood DW, Pierson EA. Homoserine lactone-mediated gene regulation in plant-associated bacteria. Annu Rev Phytopathol 1998, 36:207-225. 10.1146/annurev.phyto.36.1.207, 15012498.
53. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001, 55:165-199. 10.1146/annurev.micro.55.1.165, 11544353.
54. Nealson KH, Hastings JW. Bacterial bioluminescence its control and ecological significance. Microbiol Rev 1979, 43(4):496-518. 281490, 396467.
55. Lerat E, Moran NA. The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 2004, 21(5):903-913. 10.1093/molbev/msh097, 15014168.
56. Wang X, de Boer PAJ, Rothfield LI. A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J 1991, 10(11):3363-3372. 453064, 1915297.
57. Michael B, Smith JN, Swift S, Heffron F, Ahmer BMM. SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 2001, 183(19):5733-5742. 10.1128/JB.183.19.5733-5742.2001, 95466, 11544237.
58. Xavier KB, Bassler BL. Interference with AI-2-mediated bacterial cell-cell communication. Nature 2005, 437:750-753. 10.1038/nature03960, 1388276, 16193054.
59. Winans SC. Bacterial esperanto. Nat Struct Biol 2002, 9(2):83-84. 10.1038/nsb0202-83, 11813009.
60. Winzer K, Hardie KR, Williams P. LuxS and autoinducer-2 their contribution to quorum sensing and metabolism in bacteria. Adv Appl Microbiol 2003, 53:291-396. full_text, 14696323.
61. Rezzonico F, Duffy B. Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 2008, 8:154. 10.1186/1471-2180-8-154, 2561040, 18803868.
62. Reading NC, Sperandio V. Quorum sensing the many languages of bacteria. FEMS Microbiol Lett 2006, 254(1):1-11. 10.1111/j.1574-6968.2005.00001.x, 16451172.
63. Taga ME, Miller ST, Bassler BL. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol Microbiol 2003, 50(4):1411-1427. 10.1046/j.1365-2958.2003.03781.x, 14622426.
64. Rezzonico F, Duffy B. The role of luxS in the fire blight pathogen Erwinia amylovora is limited to metabolism and does not involve quorum sensing. Mol Plant-Microbe Interact 2007, 20(10):1284-1297. 10.1094/MPMI-20-10-1284, 17918630.
65. Expert D. Withholding and exchanging iron interactions between Erwinia spp. and their host plants. Annu Rev Phytopathol 1999, 37:307-334. 10.1146/annurev.phyto.37.1.307, 11701826.
66. Dellagi A, Brisset M-N, Paulin J-P, Expert D. Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol Plant-Microbe Interact 1998, 11(8):734-742. 10.1094/MPMI.1998.11.8.734, 9675889.
67. Kachadourian R, Dellagi A, Laurent J, Bricard L, Kunesch G, Expert D. Desferrioxamine-dependent iron transport in Erwinia amylovora CFBP 1430 cloning of the gene encoding the ferrioxamine receptor FoxR. BioMetals 1996, 9(2):143-150. 10.1007/BF00144619, 8744897.
68. Expert D, Dellagi A, Kachadourian R. Iron and fire blight role in pathogenicity of desferrioxamine E, the main siderophore of Erwinia amylovora. Fire blight the disease and its causative agent, Erwinia amylovora 2000, 179-195. Wallingford, UK CAB International, Vanneste JL.
69. Feistner GJ. Proferrioxamine synthesis in Erwinia amylovora in response to precursor or hydroxylysine feeding metabolic profiling with liquid chromatography-electrospray mass spectrometry. BioMetals 1995, 8(4):318-327. 10.1007/BF00141605, 7580052.
70. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004, 14:1394-1403. 10.1101/gr.2289704, 442156, 15231754.
71. Roselló M, Ferrer S, Llop P, López MM, Christen R, Gardan L. Description of Erwinia piriflorinigrans sp. nov., causal agent of pear blossom necrosis. Acta Hort 2008, 793:137-140.
72. Chung YR, Brenner DJ, Steigerwalt AG, Kim BS, Kim HT, Cho KY. Enterobacter pyrinus sp. nov., an organism associated with brown leaf spot disease of pear trees. Int J Syst Bacteriol 1993, 43:157-161.
73. Hao MV, Brenner DJ, Steigerwalt AG, Kosako Y, Komagata K. Erwinia persicinus a new species isolated from plants. Int J Syst Bacteriol 1990, 40:379-383.
74. Stockwell VO, Hockett K, Marie C, Duffy B. Pink Erwinia amylovora colony discoloration in diagnostic isolations by co-cultured bacteria. Acta Hort 2008, 793:539-542.
75. Jock S, Geider K. Molecular differentiation of Erwinia amylovora strains from North America and of two Asian pear pathogens by analyses of PFGE patterns and hrpN genes. Environ Microbiol 2004, 6(5):480-490. 10.1111/j.1462-2920.2004.00583.x, 15049921.
76. Geider K, Auling G, Du Z, Jakovljevic V, Jock S, Völksch B. Erwinia tasmaniensis sp. nov., a non-phytopathogenic bacterium from apple and pear trees. Int J Syst Evol Microbiol 2006, 56(12):2937-2943. 10.1099/ijs.0.64032-0, 17159002.
77. Mergaert J, Hauben L, Cnockaert MC, Swings J. Reclassification of non-pigmented Erwinia herbicola strains from trees as Erwinia billingiae sp. nov. Int J Syst Bacteriol 1999, 49:377-383.
78. Hernandez D, François P, Farinelli L, Østerås M, Schrenzel J. De novo bacterial genome sequencing millions of very short reads assembled on a desktop computer. Genome Res 2008, 18:802-809. 10.1101/gr.072033.107, 2336802, 18332092.
79. McHardy AC, Goesmann A, Pühler A, Meyer F. Development of joint application strategies for two microbial gene finders. Bioinformatics 2004, 20(10):1622-1631. 10.1093/bioinformatics/bth137, 14988122.
80. Salzberg SL, Delcher AL, Kasif S, White O. Microbial gene identification using interpolated Markov models. Nucleic Acids Res 1998, 26(2):544-548. 10.1093/nar/26.2.544, 147303, 9421513.
81. Badger JH, Olsen GJ. CRITICA coding region identification tool invoking comparative analysis. Mol Biol Evol 1999, 16(4):512-524.
82. Kanehisa M, Goto S, Kawashima S, Nakaya A. The KEGG databases at GenomeNet. Nucleic Acids Res 2002, 30(1):42-46. 10.1093/nar/30.1.42, 99091, 11752249.