1887

Abstract

Multilocus sequence analysis of Xanthomonas species revealed a very close relationship between Xanthomonas cynarae , an artichoke pathogen and Xanthomonas gardneri, a tomato and pepper pathogen. Results of whole genome sequence comparisons using average nucleotide identity between representative strains of X. gardneri and X. cynarae were well above the threshold of 95–96 %. Inoculations of X. gardneri strains in artichoke leaves caused mild disease symptoms, but only weak symptoms were observed in the bracts. Both X. cynarae and X. gardneri grew equally and caused typical bacterial spot symptoms in pepper after artificial inoculation. However, X. cynarae induced a hypersensitive reaction in tomato, while X. gardneri strains were virulent. Pathogenicity-associated gene clusters, including the protein secretion systems, type III effector profiles, and lipopolysaccharide cluster were nearly identical between the two species. Based on our results from whole genome sequence comparison, X. gardneri and X. cynarae belong to the same species. The name X. cynarae has priority and X. gardneri should be considered as a later heterotypic synonym. An emended description of X. cynarae (type strain=CFBP 4188, =DSM 16794) is given. However, due to the host specificity in artichoke and tomato, two pathovars, X. cynarae pv. cynarae and X. cynarae pv. gardneri, are proposed.

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2018-11-20
2019-10-24
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References

  1. Ridé M. Sur une maladie nouvelle de l’artichaut (Cynara scolymus). C R SeUances Acad Sci 1956;243:174–177
    [Google Scholar]
  2. Trébaol G, Gardan L, Manceau C, Tanguy JL, Tirilly Y et al. Genomic and phenotypic characterization of Xanthomonas cynarae sp. nov., a new species that causes bacterial bract spot of artichoke (Cynara scolymus L.). Int J Syst Evol Microbiol 2000;50:1471–1478 [CrossRef][PubMed]
    [Google Scholar]
  3. Potnis N, Timilsina S, Strayer A, Shantharaj D, Barak JD et al. Bacterial spot of tomato and pepper: diverse Xanthomonas species with a wide variety of virulence factors posing a worldwide challenge. Mol Plant Pathol 2015;16:907–920 [CrossRef][PubMed]
    [Google Scholar]
  4. Šutič D. Bakterioze crvenog patlidzana (Tomato bacteriosis). In Posebna Izd Inst Zasht Bilja Beograd (Special Edition)vol. 6 Beograd: Institute of Plant Protein; 1957; pp.1–65 (English summary: Rev App Mycl 36:734-735)
    [Google Scholar]
  5. Dye DW. Cultural and biochemical reaction of additional Xanthomonas species. New Zeal J Sci 1966;9:913–919
    [Google Scholar]
  6. de Ley J. Modern molecular methods in bacterial taxonomy: evaluation, application, prospects. In Proceedings of the 4th International Conference of Plant Pathogenic Bacteriavol. 1 1978; pp.347–357
    [Google Scholar]
  7. de Vos P, Goor M, Gillis M, de Ley J. Ribosomal ribonucleic acid cistron similarities of phytopathogenic Pseudomonas species. Int J Syst Bacteriol 1985;35:169–184 [CrossRef]
    [Google Scholar]
  8. Jones JB, Lacy GH, Bouzar H, Stall RE, Schaad NW. Reclassification of the xanthomonads associated with bacterial spot disease of tomato and pepper. Syst Appl Microbiol 2004;27:755–762 [CrossRef][PubMed]
    [Google Scholar]
  9. Constantin EC, Cleenwerck I, Maes M, Baeyen S, van Malderghem C et al. Genetic characterization of strains named as Xanthomonas axonopodis pv. dieffenbachiae leads to a taxonomic revision of the X. axonopodis species complex. Plant Pathol 2016;65:792–806 [CrossRef]
    [Google Scholar]
  10. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014;64:346–351 [CrossRef][PubMed]
    [Google Scholar]
  11. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 2009;106:19126–19131 [CrossRef][PubMed]
    [Google Scholar]
  12. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007;57:81–91 [CrossRef][PubMed]
    [Google Scholar]
  13. Chun J, Rainey FA. Integrating genomics into the taxonomy and systematics of the Bacteria and Archaea. Int J Syst Evol Microbiol 2014;64:316–324 [CrossRef][PubMed]
    [Google Scholar]
  14. Young JM, Park DC, Shearman HM, Fargier E. A multilocus sequence analysis of the genus Xanthomonas. Syst Appl Microbiol 2008;31:366–377 [CrossRef][PubMed]
    [Google Scholar]
  15. Merda D, Briand M, Bosis E, Rousseau C, Portier P et al. Ancestral acquisitions, gene flow and multiple evolutionary trajectories of the type three secretion system and effectors in Xanthomonas plant pathogens. Mol Ecol 2017;26:5939–5952 [CrossRef][PubMed]
    [Google Scholar]
  16. Wayne LG, Moore WEC, Stackebrandt E, Kandler O, Colwell RR et al. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Evol Microbiol 1987;37:463–464 [CrossRef]
    [Google Scholar]
  17. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017;67:1613–1617 [CrossRef][PubMed]
    [Google Scholar]
  18. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792–1797 [CrossRef][PubMed]
    [Google Scholar]
  19. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016;33:1870–1874 [CrossRef][PubMed]
    [Google Scholar]
  20. Almeida NF, Yan S, Cai R, Clarke CR, Morris CE et al. PAMDB, a multilocus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 2010;100:208–215 [CrossRef][PubMed]
    [Google Scholar]
  21. Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB et al. Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 2011;12:146 [CrossRef][PubMed]
    [Google Scholar]
  22. Markowitz VM, Chen IM, Chu K, Szeto E, Palaniappan K et al. IMG/M-HMP: a metagenome comparative analysis system for the Human Microbiome Project. PLoS One 2012;7:e40151 [CrossRef][PubMed]
    [Google Scholar]
  23. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013;14:60 [CrossRef][PubMed]
    [Google Scholar]
  24. Galán JE, Collmer A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 1999;284:1322–1328[PubMed]
    [Google Scholar]
  25. Büttner D, He SY. Type III protein secretion in plant pathogenic bacteria. Plant Physiol 2009;150:1656–1664 [CrossRef][PubMed]
    [Google Scholar]
  26. Noël L, Thieme F, Nennstiel D, Bonas U. Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol 2002;184:1340–1348 [CrossRef][PubMed]
    [Google Scholar]
  27. Block A, Li G, Fu ZQ, Alfano JR. Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 2008;11:396–403 [CrossRef][PubMed]
    [Google Scholar]
  28. Schwartz AR, Potnis N, Timilsina S, Wilson M, Patané J et al. Phylogenomics of Xanthomonas field strains infecting pepper and tomato reveals diversity in effector repertoires and identifies determinants of host specificity. Front Microbiol 2015;6:535 [CrossRef][PubMed]
    [Google Scholar]
  29. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ, Dow JM. A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 2000;38:986–1003 [CrossRef][PubMed]
    [Google Scholar]
  30. Patil PB, Sonti RV. Variation suggestive of horizontal gene transfer at a lipopolysaccharide (lps) biosynthetic locus in Xanthomonas oryzae pv. oryzae, the bacterial leaf blight pathogen of rice. BMC Microbiol 2004;4:40 [CrossRef][PubMed]
    [Google Scholar]
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