1887

Abstract

Strains of constitute a complex group of bacteria that develop within the xylem of many plant hosts, causing diseases of significant economic importance, such as Pierce’s disease in North American grapevines and citrus variegated chlorosis in Brazil. has also been obtained from other host plants, in direct correlation with the development of diseases, as in the case of coffee leaf scorch (CLS) – a disease with potential to cause severe economic losses to the Brazilian coffee industry. This paper describes a thorough genomic characterization of coffee-infecting strains, initially performed through a microarray-based approach, which demonstrated that CLS strains could be subdivided in two phylogenetically distinct subgroups. Whole-genomic sequencing of two of these bacteria (one from each subgroup) allowed identification of ORFs and horizontally transferred elements (HTEs) that were specific to CLS-related strains. Such analyses confirmed the size and importance of HTEs as major mediators of chromosomal evolution amongst these bacteria, and allowed identification of differences in gene content, after comparisons were made with previously sequenced strains, isolated from alternative hosts. Although direct experimentation still needs to be performed to elucidate the biological consequences associated with such differences, it was interesting to verify that CLS-related bacteria display variations in genes that produce toxins, as well as surface-related factors (such as fimbrial adhesins and LPS) that have been shown to be involved with recognition of specific host factors in different pathogenic bacteria.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000068
2015-05-01
2020-09-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/5/1018.html?itemId=/content/journal/micro/10.1099/mic.0.000068&mimeType=html&fmt=ahah

References

  1. Aagesen A. M., Häse C. C.. 2012; Sequence analyses of type IV pili from Vibrio cholerae, Vibrio parahaemolyticus, and Vibrio vulnificus. Microb Ecol64:509–524 [CrossRef][PubMed]
    [Google Scholar]
  2. Acuña L. G., Cárdenas J. P., Covarrubias P. C., Haristoy J. J., Flores R., Nuñez H., Riadi G., Shmaryahu A., Valdés J. et al. 2013; Architecture and gene repertoire of the flexible genome of the extreme acidophile Acidithiobacillus caldus. PLoS One8:e78237 [CrossRef][PubMed]
    [Google Scholar]
  3. Alencar V. C., Barbosa D., Santos D. S., Oliveira A. C. F., de Oliveira R. C., Nunes L. R.. 2014; Genomic sequencing of two coffee-infecting strains of Xylella fastidiosa isolated from Brazil. Genome Announc2:e01190-13 [CrossRef][PubMed]
    [Google Scholar]
  4. Almeida R. P., Nascimento F. E., Chau J., Prado S. S., Tsai C. W., Lopes S. A., Lopes J. R.. 2008; Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil. Appl Environ Microbiol74:3690–3701 [CrossRef][PubMed]
    [Google Scholar]
  5. Bhattacharyya A., Stilwagen S., Ivanova N., D’Souza M., Bernal A., Lykidis A., Kapatral V., Anderson I., Larsen N. et al. 2002; Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains. Proc Natl Acad Sci U S A99:12403–12408 [CrossRef][PubMed]
    [Google Scholar]
  6. Blumer C., Kleefeld A., Lehnen D., Heintz M., Dobrindt U., Nagy G., Michaelis K., Emödy L., Polen T. et al. 2005; Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology151:3287–3298 [CrossRef][PubMed]
    [Google Scholar]
  7. Champion O. L., Gaunt M. W., Gundogdu O., Elmi A., Witney A. A., Hinds J., Dorrell N., Wren B. W.. 2005; Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc Natl Acad Sci U S A102:16043–16048 [CrossRef][PubMed]
    [Google Scholar]
  8. Chen J., Groves R., Civerolo E. L., Viveros M., Freeman M., Zheng Y.. 2005; Two Xylella fastidiosa genotypes associated with almond leaf scorch disease on the same location in California. Phytopathology95:708–714 [CrossRef][PubMed]
    [Google Scholar]
  9. Chen J., Xie G., Han S., Chertkov O., Sims D., Civerolo E. L.. 2010; Whole genome sequences of two Xylella fastidiosa strains (M12 and M23) causing almond leaf scorch disease in California. J Bacteriol192:4534 [CrossRef][PubMed]
    [Google Scholar]
  10. Chen J., Huang H., Chang C. J., Stenger D. C.. 2013; Draft genome sequence of Xylella fastidiosa subsp. multiplex strain Griffin-1 from Quercus rubra in Georgia. Genome Announc1:e00756-13 [CrossRef][PubMed]
    [Google Scholar]
  11. Ciraulo M. B., Santos D. S., Rodrigues A. C., de Oliveira M. V., Rodrigues T., de Oliveira R. C., Nunes L. R.. 2010; Transcriptome analysis of the phytobacterium Xylella fastidiosa growing under xylem-based chemical conditions. J Biomed Biotechnol2010:781365 [CrossRef][PubMed]
    [Google Scholar]
  12. Clifford J. C., Rapicavoli J. N., Roper M. C.. 2013; A rhamnose-rich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol Plant Microbe Interact26:676–685 [CrossRef][PubMed]
    [Google Scholar]
  13. Costa H. S., Guzman A., Hernandez-Martinez R., Gispert C., Cooksey D. A.. 2006; Detection and differentiation of Xylella fastidiosa strains acquired and retained by glassy-winged sharpshooters (Hemiptera: Cicadellidae) using a mixture of strain-specific primer sets. J Econ Entomol99:1058–1064 [CrossRef][PubMed]
    [Google Scholar]
  14. Costa de Oliveira R., Yanai G. M., Muto N. H., Leite D. B., de Souza A. A., Coletta Filho H. D., Machado M. A., Nunes L. R.. 2002; Competitive hybridization on spotted microarrays as a tool to conduct comparative genomic analyses of Xylella fastidiosa strains. FEMS Microbiol Lett216:15–21 [CrossRef][PubMed]
    [Google Scholar]
  15. Cursino L., Galvani C. D., Athinuwat D., Zaini P. A., Li Y., De La Fuente L., Hoch H. C., Burr T. J., Mowery P.. 2011; Identification of an operon, Pil-Chp, that controls twitching motility and virulence in Xylella fastidiosa. Mol Plant Microbe Interact24:1198–1206 [CrossRef][PubMed]
    [Google Scholar]
  16. da Silva V. S., Shida C. S., Rodrigues F. B., Ribeiro D. C., de Souza A. A., Coletta-Filho H. D., Machado M. A., Nunes L. R., de Oliveira R. C.. 2007; Comparative genomic characterization of citrus-associated Xylella fastidiosa strains. BMC Genomics8:474 [CrossRef][PubMed]
    [Google Scholar]
  17. Darling A. E., Mau B., Perna N. T.. 2010; progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One5:e11147 [CrossRef][PubMed]
    [Google Scholar]
  18. Davis M. J., Purcell A., Thomson S. V.. 1980; Isolation medium for the Pierce’s disease bacterium. Phytopathology70:425–429 [CrossRef]
    [Google Scholar]
  19. de Lima J. E. O., Miranda V. S., Hartung J. S., Brlansky R. H., Coutinho A., Roberto S. R., Carlos E. F.. 1998; Coffee leaf scorch bacterium: Axenic culture, pathogenicity, and comparison with Xylella fastidiosa of citrus. Plant Dis82:94–97 [CrossRef]
    [Google Scholar]
  20. de Mello Varani A., Souza R. C., Nakaya H. I., de Lima W. C., Paula de Almeida L. G., Kitajima E. W., Chen J., Civerolo E., Vasconcelos A. T., Van Sluys M. A.. 2008; Origins of the Xylella fastidiosa prophage-like regions and their impact in genome differentiation. PLoS One3:e4059 [CrossRef][PubMed]
    [Google Scholar]
  21. de Souza A. A., Takita M. A., Coletta-Filho H. D., Caldana C., Goldman G. H., Yanai G. M., Muto N. H., de Oliveira R. C., Nunes L. R., Machado M. A.. 2003; Analysis of gene expression in two growth states of Xylella fastidiosa and its relationship with pathogenicity. Mol Plant Microbe Interact16:867–875 [CrossRef][PubMed]
    [Google Scholar]
  22. de Souza A. A., Takita M. A., Coletta-Filho H. D., Caldana C., Yanai G. M., Muto N. H., de Oliveira R. C., Nunes L. R., Machado M. A.. 2004; Gene expression profile of the plant pathogen Xylella fastidiosa during biofilm formation in vitro. FEMS Microbiol Lett237:341–353 [CrossRef][PubMed]
    [Google Scholar]
  23. Doddapaneni H., Yao J., Lin H., Walker M. A., Civerolo E. L.. 2006; Analysis of the genome-wide variations among multiple strains of the plant pathogenic bacterium Xylella fastidiosa. BMC Genomics7:225 [CrossRef][PubMed]
    [Google Scholar]
  24. Doddapaneni H., Francis M., Yao J., Lin H., Civerolo E.L.. 2007; Genome-wide analysis of Xylella fastidiosa: implications for detection and strain relationships. Afr J Biotechnol6:55–66
    [Google Scholar]
  25. Dorrell N., Hinchliffe S. J., Wren B. W.. 2005; Comparative phylogenomics of pathogenic bacteria by microarray analysis. Curr Opin Microbiol8:620–626 [CrossRef][PubMed]
    [Google Scholar]
  26. Felsenstein J.. 1989; phylip – Phylogeny Inference Package (Version 3.2). Cladistics5:164–166
    [Google Scholar]
  27. Fernández-Gómez B., Fernàndez-Guerra A., Casamayor E. O., González J. M., Pedrós-Alió C., Acinas S. G.. 2012; Patterns and architecture of genomic islands in marine bacteria. BMC Genomics13:347 [CrossRef][PubMed]
    [Google Scholar]
  28. Fronzes R., Remaut H., Waksman G.. 2008; Architectures and biogenesis of non-flagellar protein appendages in Gram-negative bacteria. EMBO J27:2271–2280 [CrossRef][PubMed]
    [Google Scholar]
  29. Gal-Mor O., Finlay B. B.. 2006; Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol8:1707–1719 [CrossRef][PubMed]
    [Google Scholar]
  30. Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M.. 2007; DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol57:81–91 [CrossRef][PubMed]
    [Google Scholar]
  31. Greenfield L. K., Whitfield C.. 2012; Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr Res356:12–24 [CrossRef][PubMed]
    [Google Scholar]
  32. Gu X., Glushka J., Yin Y., Xu Y., Denny T., Smith J., Jiang Y., Bar-Peled M.. 2010; Identification of a bifunctional UDP-4-keto-pentose/UDP-xylose synthase in the plant pathogenic bacterium Ralstonia solanacearum strain GMI1000, a distinct member of the 4,6-dehydratase and decarboxylase family. J Biol Chem285:9030–9040 [CrossRef][PubMed]
    [Google Scholar]
  33. Guan W., Shao J., Davis R. E., Zhao T., Huang Q.. 2014;a). Genome sequence of a Xylella fastidiosa strain causing sycamore leaf scorch disease in Virginia. Genome Announc2:e00773-14 [CrossRef][PubMed]
    [Google Scholar]
  34. Guan W., Shao J., Zhao T., Huang Q.. 2014;b). Genome sequence of a Xylella fastidiosa strain causing mulberry leaf scorch disease in Maryland. Genome Announc2:e00916-13 [CrossRef][PubMed]
    [Google Scholar]
  35. Hagemann M., Hasse D., Berg G.. 2006; Detection of a phage genome carrying a zonula occludens like toxin gene (zot) in clinical isolates of Stenotrophomonas maltophilia. Arch Microbiol185:449–458 [CrossRef][PubMed]
    [Google Scholar]
  36. Hopkins D. L.. 1989; Xylella fastidiosa: xylem-limited bacterial pathogen of plants. Annu Rev Phytopathol27:271–290 [CrossRef]
    [Google Scholar]
  37. Hopkins D. L., Purcell A. H.. 2002; Xylella fastidiosa: cause of Pierce’s disease of grapevine and other emergent diseases. Plant Dis86:1056–1066 [CrossRef]
    [Google Scholar]
  38. Howard S. L., Gaunt M. W., Hinds J., Witney A. A., Stabler R., Wren B. W.. 2006; Application of comparative phylogenomics to study the evolution of Yersinia enterocolitica and to identify genetic differences relating to pathogenicity. J Bacteriol188:3645–3653 [CrossRef][PubMed]
    [Google Scholar]
  39. Kannenberg E. L., Carlson R. W.. 2001; Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol Microbiol39:379–392 [CrossRef][PubMed]
    [Google Scholar]
  40. Kittichotirat W., Bumgarner R. E., Asikainen S., Chen C.. 2011; Identification of the pangenome and its components in 14 distinct Aggregatibacter actinomycetemcomitans strains by comparative genomic analysis. PLoS One6:e22420 [CrossRef][PubMed]
    [Google Scholar]
  41. Konstantinidis K. T., Tiedje J. M.. 2005; Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A102:2567–2572 [CrossRef][PubMed]
    [Google Scholar]
  42. Kung S. H., Almeida R. P.. 2011; Natural competence and recombination in the plant pathogen Xylella fastidiosa. Appl Environ Microbiol77:5278–5284 [CrossRef][PubMed]
    [Google Scholar]
  43. Kung S. H., Retchless A. C., Kwan J. Y., Almeida R. P.. 2013; Effects of DNA size on transformation and recombination efficiencies in Xylella fastidiosa. Appl Environ Microbiol79:1712–1717 [CrossRef][PubMed]
    [Google Scholar]
  44. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. et al. 2007; clustal w and clustal x version 2.0. Bioinformatics23:2947–2948 [CrossRef][PubMed]
    [Google Scholar]
  45. Lerouge I., Verreth C., Michiels J., Carlson R. W., Datta A., Gao M. Y., Vanderleyden J.. 2003; Three genes encoding for putative methyl- and acetyltransferases map adjacent to the wzm and wzt genes and are essential for O-antigen biosynthesis in Rhizobium etli CE3. Mol Plant Microbe Interact16:1085–1093 [CrossRef][PubMed]
    [Google Scholar]
  46. Letunic I., Bork P.. 2007; Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics23:127–128 [CrossRef][PubMed]
    [Google Scholar]
  47. Li W. B., Pria W. D. Jr, Teixeira D. C., Miranda V. S., Ayres A. J., Franco C. F., Costa M. G., He C.-X., Costa P. I., Hartung J. S.. 2001; Coffee leaf scorch caused by a strain of Xylella fastidiosa from citrus. Plant Dis85:501–505 [CrossRef]
    [Google Scholar]
  48. Li Y., Hao G., Galvani C. D., Meng Y., De La Fuente L., Hoch H. C., Burr T. J.. 2007; Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell–cell aggregation. Microbiology153:719–726 [CrossRef][PubMed]
    [Google Scholar]
  49. Margulies M., Egholm M., Altman W. E., Attiya S., Bader J. S., Bemben L. A., Berka J., Braverman M. S., Chen Y. J. et al. 2005; Genome sequencing in microfabricated high-density picolitre reactors. Nature437:376–380[PubMed]
    [Google Scholar]
  50. Marttinen P., Hanage W. P., Croucher N. J., Connor T. R., Harris S. R., Bentley S. D., Corander J.. 2012; Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res40:e6 [CrossRef][PubMed]
    [Google Scholar]
  51. Mehta A., Rosato Y. B.. 2001; Phylogenetic relationships of Xylella fastidiosa strains from different hosts, based on 16S rDNA and 16S–23S intergenic spacer sequences. Int J Syst Evol Microbiol51:311–318[PubMed]
    [Google Scholar]
  52. Mehta A., Pereira Leite R. Jr, Bomura Rosato Y.. 2001; Assessment of the genetic diversity of Xylella fastidiosa isolated from citrus in Brazil by PCR-RFLP of the 16S rDNA and 16S–23S intergenic spacer and rep-PCR fingerprinting. Antonie van Leeuwenhoek79:53–59 [CrossRef][PubMed]
    [Google Scholar]
  53. Meng Y., Li Y., Galvani C. D., Hao G., Turner J. N., Burr T. J., Hoch H. C.. 2005; Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J Bacteriol187:5560–5567 [CrossRef][PubMed]
    [Google Scholar]
  54. Nguyen L. C., Taguchi F., Tran Q. M., Naito K., Yamamoto M., Ohnishi-Kameyama M., Ono H., Yoshida M., Chiku K. et al. 2012; Type IV pilin is glycosylated in Pseudomonas syringae pv. tabaci 6605 and is required for surface motility and virulence. Mol Plant Pathol13:764–774 [CrossRef][PubMed]
    [Google Scholar]
  55. Nunes L. R., Rosato Y. B., Muto N. H., Yanai G. M., da Silva V. S., Leite D. B., Gonçalves E. R., de Souza A. A., Coletta-Filho H. D. et al. 2003; Microarray analyses of Xylella fastidiosa provide evidence of coordinated transcription control of laterally transferred elements. Genome Res13:570–578 [CrossRef][PubMed]
    [Google Scholar]
  56. Nunney L., Yuan X., Bromley R., Hartung J., Montero-Astúa M., Moreira L., Ortiz B., Stouthamer R.. 2010; Population genomic analysis of a bacterial plant pathogen: novel insight into the origin of Pierce’s disease of grapevine in the U.S.. PLoS One5:e15488 [CrossRef][PubMed]
    [Google Scholar]
  57. Nunney L., Yuan X., Bromley R. E., Stouthamer R.. 2012; Detecting genetic introgression: high levels of intersubspecific recombination found in Xylella fastidiosa in Brazil. Appl Environ Microbiol78:4702–4714 [CrossRef][PubMed]
    [Google Scholar]
  58. Ochman H., Lawrence J. G., Groisman E. A.. 2000; Lateral gene transfer and the nature of bacterial innovation. Nature405:299–304 [CrossRef][PubMed]
    [Google Scholar]
  59. Oresnik I. J., Twelker S., Hynes M. F.. 1999; Cloning and characterization of a Rhizobium leguminosarum gene encoding a bacteriocin with similarities to RTX toxins. Appl Environ Microbiol65:2833–2840[PubMed]
    [Google Scholar]
  60. Paradela-Filho O., Sugimori M. H., Ribeiro I. J. A., Garcia A.., Jr Beretta M. J. G., Harakawa R., Machado M. A., Laranjeira F.F, Rodrigues Neto J., Beriam L. O. S.. 1997; Occurrence of Xylella fastidiosa in coffee plants in Brazil. Summa Phytopathol23:46–49
    [Google Scholar]
  61. Pieretti I., Royer M., Barbe V., Carrere S., Koebnik R., Cociancich S., Couloux A., Darrasse A., Gouzy J. et al. 2009; The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics10:616 [CrossRef][PubMed]
    [Google Scholar]
  62. Pooler M. R., Hartung J. S.. 1995; Specific PCR detection and identification of Xylella fastidiosa strains causing citrus variegated chlorosis. Curr Microbiol31:377–381 [CrossRef][PubMed]
    [Google Scholar]
  63. Puvirajesinghe T. M., Elantak L., Lignon S., Franche N., Ilbert M., Ansaldi M.. 2012; DnaJ (Hsp40 protein) binding to folded substrate impacts KplE1 prophage excision efficiency. J Biol Chem287:14169–14177 [CrossRef][PubMed]
    [Google Scholar]
  64. Richter M., Rosselló-Móra R.. 2009; Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  65. Rocha J. G., Zambolim L., Zambolim E. M., Ribeiro do Vale F. X., Junior W. C. J., Filho A. B.. 2010; Quantification of yield loss due to coffee leaf scorch. Crop Prot29:1100–1104 [CrossRef]
    [Google Scholar]
  66. Ronquist F., Huelsenbeck J. P.. 2003; MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics19:1572–1574 [CrossRef][PubMed]
    [Google Scholar]
  67. Roper M. C., Greve L. C., Warren J. G., Labavitch J. M., Kirkpatrick B. C.. 2007; Xylella fastidiosa requires polygalacturonase for colonization and pathogenicity in Vitis vinifera grapevines. Mol Plant Microbe Interact20:411–419 [CrossRef][PubMed]
    [Google Scholar]
  68. Saeed A. I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T. et al. 2003; tm4: a free, open-source system for microarray data management and analysis. Biotechniques34:374–378[PubMed]
    [Google Scholar]
  69. Schaad N. W., Postnikova E., Lacy G., Fatmi M., Chang C. J.. 2004; Xylella fastidiosa subspecies: X. fastidiosa subsp. [correction] fastidiosa [correction] subsp. nov., X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. nov.. Syst Appl Microbiol27:290–300 [CrossRef][PubMed]
    [Google Scholar]
  70. Schreiber I. V., Koiral H., Lara M., Ojeda A., Dowd M., Bextin S. E., Moran L.. 2010; Unraveling the first Xylella fastidiosa subsp. fastidiosa genome from Texas. Southwest Entomologist35:479–483 [CrossRef]
    [Google Scholar]
  71. Simpson A. J., Reinach F. C., Arruda P., Abreu F. A., Acencio M., Alvarenga R., Alves L. M., Araya J. E., Baia G. S. et al. 2000; The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature406:151–159 [CrossRef][PubMed]
    [Google Scholar]
  72. Su C. C., Deng W. L., Jan F. J., Chang C. J., Huang H., Chen J.. 2014; Draft genome sequence of Xylella fastidiosa pear leaf scorch strain in Taiwan. Genome Announc2:e00166-14 [CrossRef][PubMed]
    [Google Scholar]
  73. Sun Q., Greve L. C., Labavitch J. M.. 2011; Polysaccharide compositions of intervessel pit membranes contribute to Pierce’s disease resistance of grapevines. Plant Physiol155:1976–1987 [CrossRef][PubMed]
    [Google Scholar]
  74. Thanweer F., Tahiliani V., Korres H., Verma N. K.. 2008; Topology and identification of critical residues of the O-acetyltransferase of serotype-converting bacteriophage, SF6, of Shigella flexneri. Biochem Biophys Res Commun375:581–585 [CrossRef][PubMed]
    [Google Scholar]
  75. van Kessel J. C., Ulrich L. E., Zhulin I. B., Bassler B. L.. 2013; Analysis of activator and repressor functions reveals the requirements for transcriptional control by LuxR, the master regulator of quorum sensing in Vibrio harveyi. MBio4:e00378-13 [CrossRef][PubMed]
    [Google Scholar]
  76. Van Sluys M. A., de Oliveira M. C., Monteiro-Vitorello C. B., Miyaki C. Y., Furlan L. R., Camargo L. E., da Silva A. C., Moon D. H., Takita M. A. et al. 2003; Comparative analyses of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol185:1018–1026 [CrossRef][PubMed]
    [Google Scholar]
  77. Varani A. M., Monteiro-Vitorello C. B., de Almeida L. G., Souza R. C., Cunha O. L., Lima W. C., Civerolo E., Van Sluys M. A., Vasconcelos A. T.. 2012; Xylella fastidiosa comparative genomic database is an information resource to explore the annotation, genomic features, and biology of different strains. Genet Mol Biol35:149–152 [CrossRef][PubMed]
    [Google Scholar]
  78. Varani A. M., Monteiro-Vitorello C. B., Nakaya H. I., Van Sluys M. A.. 2013; The role of prophage in plant-pathogenic bacteria. Annu Rev Phytopathol51:429–451 [CrossRef][PubMed]
    [Google Scholar]
  79. Weissman S. J., Chattopadhyay S., Aprikian P., Obata-Yasuoka M., Yarova-Yarovaya Y., Stapleton A., Ba-Thein W., Dykhuizen D., Johnson J. R., Sokurenko E. V.. 2006; Clonal analysis reveals high rate of structural mutations in fimbrial adhesins of extraintestinal pathogenic Escherichia coli. Mol Microbiol59:975–988 [CrossRef][PubMed]
    [Google Scholar]
  80. Wells J. M., Raju B. C., Hung H. Y., Weisburg W. G., Mandelco-Paul L., Brenner D. J.. 1987; Xylella fastidiosa gen. nov., sp. nov: Gram negative xylem-limited fastidious plant bacteria related to Xanthomonas spp.. Int J Syst Evol Bacteriol37:136–143 [CrossRef]
    [Google Scholar]
  81. Zhang S., Flores-Cruz Z., Kumar D., Chakrabarty P., Hopkins D. L., Gabriel D. W.. 2011; The Xylella fastidiosa biocontrol strain EB92-1 genome is very similar and syntenic to Pierce’s disease strains. J Bacteriol193:5576–5577 [CrossRef][PubMed]
    [Google Scholar]
  82. Zhou Y., Liang Y., Lynch K. H., Dennis J. J., Wishart D. S.. 2011; phast: a fast phage search tool. Nucleic Acids Res39:Web Server issueW347–W352 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000068
Loading
/content/journal/micro/10.1099/mic.0.000068
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error