1887

Abstract

We describe a novel species isolated from walnut () which comprises non-pathogenic and pathogenic strains on walnut. The isolates, obtained from a single ornamental walnut tree showing disease symptoms, grew on yeast extract–dextrose–carbonate agar as mucoid yellow colonies characteristic of species. Pathogenicity assays showed that while strain CPBF 424 causes disease in walnut, strain CPBF 367 was non-pathogenic on walnut leaves. Biolog GEN III metabolic profiles disclosed some differences between strains CPBF 367 and CPBF 424 and other xanthomonads. Multilocus sequence analysis with seven housekeeping genes (, , , , , , ) grouped these strains in a distinct cluster from pv. and closer to and pv. . Average nucleotide identity (ANI) analysis results displayed similarity values below 93 % to strains. Meanwhile ANI and digital DNA–DNA hybridization similarity values were below 89 and 50 % to non- strains, respectively, revealing that they do not belong to any previously described species. Furthermore, the two strains show over 98 % similarity to each other. Genomic analysis shows that strain CPBF 424 harbours a complete type III secretion system and several type III effector proteins, in contrast with strain CPBF 367, shown to be non-pathogenic in plant bioassays. Taking these data altogether, we propose that strains CPBF 367 and CPBF 424 belong to a new species herein named sp. nov., with CPBF 424 (=LMG 31037=CCOS 1891=NCPPB 4675) as the type strain.

Funding
This study was supported by the:
  • European Cooperation in Science and Technology (Award COST Action CA16107)
    • Principle Award Recipient: Not Applicable
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Award IZCOZ0_177064)
    • Principle Award Recipient: Nay C. Dia
  • Fundação para a Ciência e a Tecnologia (Award Project EVOXANT (PTDC/BIA-EVF/3635/2014-POCI-01-0145-FEDER-016600))
    • Principle Award Recipient: Fernando Tavares
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004386
2020-09-14
2021-10-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/70/12/6024.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.004386&mimeType=html&fmt=ahah

References

  1. Vauterin L, Rademaker J, Swings J. Synopsis on the taxonomy of the genus Xanthomonas . Phytopathology 2000; 90:677–682 [View Article][PubMed]
    [Google Scholar]
  2. Vauterin L, Hoste B, Kersters K, Swings J. Reclassification of Xanthomonas . Int J Syst Bacteriol 1995; 45:472–489 [View Article]
    [Google Scholar]
  3. da Gama MAS, Barbosa MAG, de Farias ARG, da Silva Júnior WJ, Mariano R de LR. Taxonomic repositioning of Xanthomonas campestris pv. viticola (Nayudu 1972) Dye 1978 as Xanthomonas citri pv. viticola (Nayudu 1972) Dye 1978 comb. nov. and emendation of the description of Xanthomonas citri pv. anacardii to include pigmented isolates pathogenic to cashew plant. Phytopathology 2018; 108:1143–1153
    [Google Scholar]
  4. 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 [View Article]
    [Google Scholar]
  5. Vicente JG, Rothwell S, Holub EB, Studholme DJ. Pathogenic, phenotypic and molecular characterisation of Xanthomonas nasturtii sp. nov. and Xanthomonas floridensis sp. nov., new species of Xanthomonas associated with watercress production in Florida. Int J Syst Evol Microbiol 2017; 67:3645–3654 [View Article][PubMed]
    [Google Scholar]
  6. López MM, Lopez-Soriano P, Garita-Cambronero J, Beltrán C, Taghouti G et al. Xanthomonas prunicola sp. nov., a novel pathogen that affects nectarine (Prunus persica var. nectarina) trees. Int J Syst Evol Microbiol 2018; 68:1857–1866 [View Article][PubMed]
    [Google Scholar]
  7. Triplett LR, Verdier V, Campillo T, Van Malderghem C, Cleenwerck I et al. Characterization of a novel clade of Xanthomonas isolated from rice leaves in Mali and proposal of Xanthomonas maliensis sp. nov. Antonie van Leeuwenhoek 2015; 107:869–881 [View Article][PubMed]
    [Google Scholar]
  8. Jacques M-A, Arlat M, Boulanger A, Boureau T, Carrère S et al. Using Ecology, Physiology, and Genomics to Understand Host Specificity in Xanthomonas . Annu Rev Phytopathol 2016; 54:163–187 [View Article][PubMed]
    [Google Scholar]
  9. Essakhi S, Cesbron S, Fischer-Le Saux M, Bonneau S, Jacques M-A et al. Phylogenetic and variable-number tandem-repeat analyses identify nonpathogenic Xanthomonas arboricola lineages lacking the canonical type III secretion system. Appl Environ Microbiol 2015; 81:5395–5410 [View Article][PubMed]
    [Google Scholar]
  10. Garita-Cambronero J, Palacio-Bielsa A, López MM, Cubero J. Comparative genomic and phenotypic characterization of pathogenic and non-pathogenic strains of Xanthomonas arboricola reveals insights into the infection process of bacterial spot disease of stone fruits. PLoS One 2016; 11:e0161977 [View Article][PubMed]
    [Google Scholar]
  11. Merda D, Bonneau S, Guimbaud J-F, Durand K, Brin C et al. Recombination-prone bacterial strains form a reservoir from which epidemic clones emerge in agroecosystems. Environ Microbiol Rep 2016; 8:572–581 [View Article][PubMed]
    [Google Scholar]
  12. Yeates GW. A proposed nomenclature and classification for plant pathogenic bacteria. New Zeal J Agric Res 1978; 21:153–177
    [Google Scholar]
  13. Schulze-Lefert P, Panstruga R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 2011; 16:117–125 [View Article][PubMed]
    [Google Scholar]
  14. Fernandes C, Sousa R, Tavares F, Cruz L. First Report of Xanthomonas arboricola causing bacterial blight on pecan trees in Portugal. Plant Disease 2018; 102:2632 [View Article]
    [Google Scholar]
  15. Lamichhane JR. Xanthomonas arboricola diseases of stone fruit, almond, and walnut trees: Progress toward understanding and management. Plant Dis 2014; 98:1600–1610 [View Article][PubMed]
    [Google Scholar]
  16. Leslie C, Uratsu S, McGranahan G, Dandekar A. Agrobacterium protocols volume 2. Springer 2006
    [Google Scholar]
  17. Belisario A, Santori A, Potente G, Fiorin A, Saphy B et al. Brown apical necrosis (BAN): a fungal disease causing fruit drop of english walnut. In Neil MC. editor Vi International Walnut Symposium (Acta Horticulturae. Leuven 1: International Society of Horticultural Science 2010 pp 449–452 [View Article]
    [Google Scholar]
  18. Moragrega C, Matias J, Aletà N, Montesinos E, Rovira M. Apical necrosis and premature drop of Persian (English) walnut fruit caused by Xanthomonas arboricola pv. juglandis . Plant Dis 2011; 95:1565–1570 [View Article][PubMed]
    [Google Scholar]
  19. Hajri A, Meyer D, Delort F, Guillaumès J, Brin C et al. Identification of a genetic lineage within Xanthomonas arboricola pv. juglandis as the causal agent of vertical oozing canker of Persian (English) walnut in France. Plant Pathol 2010; 59:1014–1022 [View Article]
    [Google Scholar]
  20. Fernandes C, Albuquerque P, Cruz L, Tavares F. Genotyping and epidemiological metadata provides new insights into population structure of Xanthomonas isolated from walnut trees.
  21. Fernandes C, Albuquerque P, Sousa R, Cruz L, Tavares F. Multiple DNA markers for identification of Xanthomonas arboricola pv. juglandis isolates and its direct detection in plant samples. Plant Dis 2017; 101:858–865 [View Article][PubMed]
    [Google Scholar]
  22. Stolp H, Starr MP. Bacteriophage reactions and speciation of Phytopathogenic Xanthomonads . J Phytopathol 1964; 51:442–478 [View Article]
    [Google Scholar]
  23. International Seed Testing Association International rules for seed testing rules. Seed Sci Technol 1999; 27:
    [Google Scholar]
  24. Fischer-Le Saux M, Bonneau S, Essakhi S, Manceau C, Jacques M-A. Aggressive emerging pathovars of Xanthomonas arboricola represent widespread epidemic clones distinct from poorly pathogenic strains, as revealed by multilocus sequence typing. Appl Environ Microbiol 2015; 81:4651–4668 [View Article][PubMed]
    [Google Scholar]
  25. Fernandes C, Blom J, Pothier JF, Tavares F. High-quality draft genome sequence of Xanthomonas sp. strain CPBF 424, a Walnut-Pathogenic strain with atypical features. Microbiol Resour Announc 2018; 7: [View Article][PubMed]
    [Google Scholar]
  26. Blom J, Albaum SP, Doppmeier D, Pühler A, Vorhölter F-J et al. EDGAR: a software framework for the comparative analysis of prokaryotic genomes. BMC Bioinformatics 2009; 10:154 [View Article][PubMed]
    [Google Scholar]
  27. Blom J, Kreis J, Spänig S, Juhre T, Bertelli C et al. EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 2016; 44:W22–W28 [View Article][PubMed]
    [Google Scholar]
  28. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article][PubMed]
    [Google Scholar]
  29. Richter M, Rosselló-Móra R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 2009; 106:19126–19131 [View Article][PubMed]
    [Google Scholar]
  30. Hajri A, Pothier JF, Fischer-Le Saux M, Bonneau S, Poussier S et al. Type three effector gene distribution and sequence analysis provide new insights into the pathogenicity of plant-pathogenic Xanthomonas arboricola . Appl Environ Microbiol 2012; 78:371–384 [View Article][PubMed]
    [Google Scholar]
  31. Ryan RP, Vorhölter F-J, Potnis N, Jones JB, Van Sluys M-A et al. Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. Nat Rev Microbiol 2011; 9:344–355 [View Article][PubMed]
    [Google Scholar]
  32. White FF, Potnis N, Jones JB, Koebnik R. The type III effectors of Xanthomonas . Mol Plant Pathol 2009; 10:749–766 [View Article][PubMed]
    [Google Scholar]
  33. Cesbron S, Briand M, Essakhi S, Gironde S, Boureau T et al. Comparative genomics of pathogenic and nonpathogenic strains of Xanthomonas arboricola unveil molecular and evolutionary events linked to pathoadaptation. Front Plant Sci 2015; 6:1126 [View Article][PubMed]
    [Google Scholar]
  34. Garita-Cambronero J, Palacio-Bielsa A, Cubero J. Xanthomonas arboricola pv. pruni, causal agent of bacterial spot of stone fruits and almond: its genomic and phenotypic characteristics in the X. arboricola species context. Mol Plant Pathol 2018; 19:2053–2065 [View Article][PubMed]
    [Google Scholar]
  35. Garita-Cambronero J, Palacio-Bielsa A, López MM, Cubero J. Pan-genomic analysis permits differentiation of virulent and non-virulent strains of Xanthomonas arboricola that cohabit Prunus spp. and elucidate bacterial virulence factors. Front Microbiol 2017; 8:1–17 [View Article]
    [Google Scholar]
  36. Guo Y, Figueiredo F, Jones J, Wang N. HrpG and HrpX play global roles in coordinating different virulence traits of Xanthomonas axonopodis pv. citri . Mol Plant Microbe Interact 2011; 24:649–661 [View Article][PubMed]
    [Google Scholar]
  37. Jacobs JM, Pesce C, Lefeuvre P, Koebnik R. Comparative genomics of a cannabis pathogen reveals insight into the evolution of pathogenicity in Xanthomonas . Front Plant Sci 2015; 6:431 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004386
Loading
/content/journal/ijsem/10.1099/ijsem.0.004386
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month Most Cited RSS feed

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