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Abstract

The UK Plant Health Risk Register (PHRR) lists bacterial pathogens of regulatory concern, but genome sequences – particularly for type and pathotype strains – are lacking for several taxa. We surveyed 59 bacterial taxa listed in the PHRR and identified key gaps in publicly available genome data for those taxa. To address these, we sequenced 17 bacterial strains from the National Collection of Plant Pathogenic Bacteria (NCPPB), using Illumina and Oxford Nanopore technologies to assemble complete, chromosome-level sequences. Newly sequenced genomes include type strains NCPPB 4602, NCPPB 929 and NCPPB 4692 in addition to pathotype strains pv. NCPPB 935, pv. NCPPB 416, pv. NCPPB 581 and pv. NCPPB 2372. Also included were non-type strains: subsp. (NCPPB 3725, 3727 and 3728), three strains received as pv. (NCPPB 1939 and 3948) and five strains of pv. (NCPPB 3886, 3887, 3797, 3795 and 3796). These bacterial genome sequences have relevance for global microbiology and plant pathology communities beyond the UK. All data have been deposited in public repositories. These genomes will help support taxonomy, molecular assay development and plant health surveillance. Data are publicly available under BioProject accessions PRJNA1126170, PRJNA1127186, PRJNA1127218, PRJNA1129842, PRJNA1129913 and PRJNA1130007.

Funding
This study was supported by the:
  • Wellcome Trust (Award 218247/Z/19/Z)
    • Principal Award Recipient: NotApplicable
  • Biotechnology and Biological Sciences Research Council (Award BB/W018853/1)
    • Principal Award Recipient: DavidStudholme
  • Biotechnology and Biological Sciences Research Council (Award BB/T010916/1)
    • Principal Award Recipient: DavidStudholme
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2025-11-19
2025-12-16

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References

  1. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 2012; 13:614–629 [View Article] [PubMed]
    [Google Scholar]
  2. Xu J, Wang N. Where are we going with genomics in plant pathogenic bacteria?. Genomics 2019; 111:729–736 [View Article]
    [Google Scholar]
  3. Catara V, Cubero J, Pothier JF, Bosis E, Bragard C et al. Trends in Molecular diagnosis and diversity studies for phytosanitary regulated Xanthomonas. Microorganisms 2021; 9:862 [View Article] [PubMed]
    [Google Scholar]
  4. Hugenholtz P, Chuvochina M, Oren A, Parks DH, Soo RM. Prokaryotic taxonomy and nomenclature in the age of big sequence data. ISME J 2021; 15:1879–1892 [View Article]
    [Google Scholar]
  5. Federhen S. Type material in the NCBI taxonomy database. Nucleic Acids Res 2015; 43:D1086–98 [View Article] [PubMed]
    [Google Scholar]
  6. Wu L, Ma J. The Global Catalogue of Microorganisms (GCM) 10K type strain sequencing project: providing services to taxonomists for standard genome sequencing and annotation. Int J Syst Evol Microbiol 2019; 69:895–898 [View Article] [PubMed]
    [Google Scholar]
  7. Ahmed FA, Larrea-Sarmiento A, Alvarez AM, Arif M. Genome-informed diagnostics for specific and rapid detection of Pectobacterium species using recombinase polymerase amplification coupled with a lateral flow device. Sci Rep 2018; 8:15972 [View Article] [PubMed]
    [Google Scholar]
  8. Stulberg MJ, Santillana G, Studholme DJ, Kasiborski B, Ortiz-Castro M et al. Genomics-informed molecular detection of Xanthomonas vasicola pv. vasculorum strains causing severe bacterial leaf streak of corn. Phytopathology 2020; 110:1174–1179 [View Article] [PubMed]
    [Google Scholar]
  9. Bull CT, de Boer SH, Denny P, Firrao G, Fischer-Le saux M et al. Demystifying the nomenclature of bacterial plant pathogens. J Plant Pathol 2008; 90:403–417
    [Google Scholar]
  10. Schwartz AR, Potnis N, Timilsina S, Wilson M, Patane 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: [View Article]
    [Google Scholar]
  11. Roach R, Mann R, Gambley CG, Chapman T, Shivas RG et al. Genomic sequence analysis reveals diversity of Australian Xanthomonas species associated with bacterial leaf spot of tomato, capsicum and chilli. BMC Genomics 2019; 20:310 [View Article] [PubMed]
    [Google Scholar]
  12. Timilsina S, Abrahamian P, Potnis N, Minsavage GV, White FF et al. Analysis of sequenced genomes of Xanthomonas perforans identifies candidate targets for resistance breeding in tomato. Phytopathology 2016; 106:1097–1104 [View Article] [PubMed]
    [Google Scholar]
  13. Klein-Gordon JM, Timilsina S, Xing Y, Abrahamian P, Garrett KA et al. Whole genome sequences reveal the Xanthomonas perforans population is shaped by the tomato production system. ISME J 2022; 16:591–601 [View Article] [PubMed]
    [Google Scholar]
  14. Goig GA, Blanco S, Garcia-Basteiro AL, Comas I. Contaminant DNA in bacterial sequencing experiments is a major source of false genetic variability. BMC Biol 2020; 18:24 [View Article]
    [Google Scholar]
  15. Lau KA, Gonçalves da Silva A, Theis T, Gray J, Ballard SA et al. Proficiency testing for bacterial whole genome sequencing in assuring the quality of microbiology diagnostics in clinical and public health laboratories. Pathology 2021; 53:902–911 [View Article] [PubMed]
    [Google Scholar]
  16. Schiavone A, Pugliese N, Samarelli R, Cumbo C, Minervini CF et al. Factors affecting the quality of bacterial genomes assemblies by canu after nanopore sequencing. Appl Sci 2022; 12:3110 [View Article]
    [Google Scholar]
  17. Studholme DJ. Genome update. let the consumer beware: streptomyces genome sequence quality. Microb Biotechnol 2016; 9:3–7 [View Article]
    [Google Scholar]
  18. Kitts PA, Church DM, Thibaud-Nissen F, Choi J, Hem V et al. Assembly: a resource for assembled genomes at NCBI. Nucleic Acids Res 2016; 44:D73–80 [View Article] [PubMed]
    [Google Scholar]
  19. Koren S, Phillippy AM. One chromosome, one contig: complete microbial genomes from long-read sequencing and assembly. Curr Opin Microbiol 2015; 23:110–120 [View Article] [PubMed]
    [Google Scholar]
  20. Liao X, Li M, Zou Y, Wu FX et al. Current challenges and solutions of de novo assembly. Quant Biol 2019; 7:90–109 [View Article]
    [Google Scholar]
  21. Nagarajan N, Pop M. Sequence assembly demystified. Nat Rev Genet 2013; 14:157–167 [View Article] [PubMed]
    [Google Scholar]
  22. Bouras G, Judd LM, Edwards RA, Vreugde S, Stinear TP et al. How low can you go? Short-read polishing of Oxford Nanopore bacterial genome assemblies. Microb Genom 2024; 10:001254 [View Article] [PubMed]
    [Google Scholar]
  23. Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genom 2017; 3:e000132 [View Article] [PubMed]
    [Google Scholar]
  24. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  25. Tørresen OK, Star B, Mier P, Andrade-Navarro MA, Bateman A et al. Tandem repeats lead to sequence assembly errors and impose multi-level challenges for genome and protein databases. Nucleic Acids Res 2019; 47:10994–11006 [View Article] [PubMed]
    [Google Scholar]
  26. Boch J, Bonas U, Lahaye T. TAL effectors--pathogen strategies and plant resistance engineering. New Phytol 2014; 204:823–832 [View Article] [PubMed]
    [Google Scholar]
  27. Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ. TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol 2013; 23:390–398 [View Article] [PubMed]
    [Google Scholar]
  28. Mak AN-S, Bradley P, Bogdanove AJ, Stoddard BL. TAL effectors: function, structure, engineering and applications. Curr Opin Struct Biol 2013; 23:93–99 [View Article]
    [Google Scholar]
  29. Scholze H, Boch J. TAL effectors are remote controls for gene activation. Curr Opin Microbiol 2011; 14:47–53 [View Article]
    [Google Scholar]
  30. Erkes A, Grove RP, Žarković M, Krautwurst S, Koebnik R et al. Assembling highly repetitive Xanthomonas TALomes using Oxford Nanopore sequencing. BMC Genomics 2023; 24:151 [View Article] [PubMed]
    [Google Scholar]
  31. Peng Z, Hu Y, Xie J, Potnis N, Akhunova A et al. Long read and single molecule DNA sequencing simplifies genome assembly and TAL effector gene analysis of Xanthomonas translucens. BMC Genomics 2016; 17:21 [View Article] [PubMed]
    [Google Scholar]
  32. Baker RHA, Anderson H, Bishop S, MacLeod A, Parkinson N et al. The UK plant health risk register: a tool for prioritizing actions. EPPO Bulletin 2014; 44:187–194 [View Article]
    [Google Scholar]
  33. Malik KA, Claus D. Bacterial culture collections: their importance to biotechnology and microbiology. Biotechnol Genet Eng Rev 1987; 5:137–197 [View Article] [PubMed]
    [Google Scholar]
  34. Barba M, Van den Bergh I, Belisario A, Beed F. The need for culture collections to support plant pathogen diagnostic networks. Res Microbiol 2010; 161:472–479 [View Article] [PubMed]
    [Google Scholar]
  35. Sayers EW, Bolton EE, Brister JR, Canese K, Chan J et al. Database resources of the national center for biotechnology information. Nucleic Acids Res 2022; 50:D20–D26 [View Article]
    [Google Scholar]
  36. Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD et al. GenBank. Nucleic Acids Res 2019; 47:D94–D99 [View Article]
    [Google Scholar]
  37. Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 2016; 44:6614–6624 [View Article] [PubMed]
    [Google Scholar]
  38. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  39. Balaž J, Iličić R, Ognjanov V, Ivanović Ž, Popović T. Epidemiology studies of pseudomonas syringae pathovars associated with bacterial canker on the sweet cherry in serbia. J Plant Pathol 2016; 98:285–294 [View Article]
    [Google Scholar]
  40. Bultreys A, Kaluzna M. Bacterial cankers caused by Pseudomonas syringae on stone fruit species with special emphasis on the pathovars syringae and morsprunorum race 1 and race 2. J Plant Pathol 2010; 92:S21–S33
    [Google Scholar]
  41. Díaz D, Zamorano A, García H, Ramos C, Cui W et al. Development of a genome-informed protocol for detection of Pseudomonas amygdali pv. morsprunorum Using LAMP and PCR. Plants 2023; 12:4119 [View Article] [PubMed]
    [Google Scholar]
  42. Gilbert V, Legros F, Maraite H, Bultreys A. Genetic analyses of Pseudomonas syringae isolates from Belgian fruit orchards reveal genetic variability and isolate-host relationships within the pathovar syringae, and help identify both races of the pathovar morsprunorum. Eur J Plant Pathol 2009; 124:199–218 [View Article]
    [Google Scholar]
  43. Iličić R, Balaž J, Ognjanov V, Popović T. Epidemiology studies of Pseudomonas syringae pathovars associated with bacterial canker on the sweet cherry in Serbia. Plant Prot Sci 2021; 57:196–205 [View Article]
    [Google Scholar]
  44. Roos I, Hattingh M. Bacterial canker of sweet cherry in south africa. Phytophylactica 1986; 18:1–4
    [Google Scholar]
  45. Vicente JG, Alves JP, Russell K, Roberts SJ. Identification and discrimination of Pseudomonas syringae isolates from Wild Cherry in England. Eur J Plant Pathol 2004; 110:337–351 [View Article]
    [Google Scholar]
  46. Gardan L, Shafik H, Belouin S, Broch R, Grimont F et al. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int J Syst Bacteriol 1999; 49 Pt 2:469–478 [View Article] [PubMed]
    [Google Scholar]
  47. Hulin MT, Mansfield JW, Brain P, Xu X, Jackson RW et al. Characterization of the pathogenicity of strains of Pseudomonas syringae towards cherry and plum. Plant Pathol 2018; 67:1177–1193 [View Article] [PubMed]
    [Google Scholar]
  48. Manna S, Santander RD, Zhao Y. First report of Pseudomonas amygdali pv. morsprunorum causing bacterial canker in sweet cherry orchards in Washington State. Plant Disease 2024; 108:2560 [View Article]
    [Google Scholar]
  49. Gomila M, Busquets A, Mulet M, García-Valdés E, Lalucat J. Clarification of taxonomic status within the Pseudomonas syringae species group based on a phylogenomic analysis. Front Microbiol 2017; 8:2422 [View Article]
    [Google Scholar]
  50. Bull CT, Boer SH, Denny TP, Firrao G, Saux M-L et al. Comprehensive list of names of plant pathogenic bacteria, 1980-2007. J Plant Pathol 2010; 92:551–592
    [Google Scholar]
  51. Young JM, Bradbury JF, Davis RE, Dickey RS, Ercolani GL et al. Nomenclatural revisions of plant pathogenic bacteria and list of names 1980-1988. Rev Plant Pathol 1991; 70:211–221
    [Google Scholar]
  52. Ménard M, Sutra L, Luisetti J, Prunier JP, Gardan L. Pseudomonas syringae pv. avii (pv. nov.), the causal agent of bacterial canker of wild cherries (Prunus avium) in France. Eur J Plant Pathol 2003; 109:565–576 [View Article]
    [Google Scholar]
  53. Hulin MT, Armitage AD, Vicente JG, Holub EB, Baxter L et al. Comparative genomics of Pseudomonas syringae reveals convergent gene gain and loss associated with specialization onto cherry (Prunus avium). New Phytol 2018; 219:672–696 [View Article]
    [Google Scholar]
  54. Federhen S. The NCBI taxonomy database. Nucleic Acids Res 2012; 40:D136–43 [View Article] [PubMed]
    [Google Scholar]
  55. Barton IS, Fuqua C, Platt TG. Ecological and evolutionary dynamics of a model facultative pathogen: Agrobacterium and crown gall disease of plants. Environ Microbiol 2018; 20:16–29 [View Article] [PubMed]
    [Google Scholar]
  56. Weisberg AJ, Wu Y, Chang JH, Lai E-M, Kuo C-H. Virulence and ecology of agrobacteria in the context of evolutionary genomics. Annu Rev Phytopathol 2023; 61:1–23 [View Article] [PubMed]
    [Google Scholar]
  57. Kuzmanović N, Puławska J, Hao L, Burr TJ. The ecology of Agrobacterium vitis and management of crown gall disease in vineyards. Curr Top Microbiol Immunol 2018; 418:15–53 [View Article] [PubMed]
    [Google Scholar]
  58. Kuzmanović N, Puławska J, Prokić A, Ivanović M, Zlatković N et al. Agrobacterium arsenijevicii sp. nov., isolated from crown gall tumors on raspberry and cherry plum. Syst Appl Microbiol 2015; 38:373–378 [View Article] [PubMed]
    [Google Scholar]
  59. Nabhan S, De Boer SH, Maiss E, Wydra K. Pectobacterium aroidearum sp. nov., a soft rot pathogen with preference for monocotyledonous plants. Int J Syst Evol Microbiol 2013; 63:2520–2525 [View Article] [PubMed]
    [Google Scholar]
  60. Safni I, Cleenwerck I, De Vos P, Fegan M, Sly L et al. Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia syzygii subsp. indonesiensis subsp. nov., banana blood disease bacterium strains as Ralstonia syzygii subsp. celebesensis subsp. nov. and R. solanacearum phylotype I and III strains as Ralstonia pseudosolanacearum sp. nov. Int J Syst Evol Microbiol 2014; 64:3087–3103 [View Article] [PubMed]
    [Google Scholar]
  61. Kurm V, Houwers I, Coipan CE, Bonants P, Waalwijk C et al. Whole genome characterization of strains belonging to the Ralstonia solanacearum species complex and in silico analysis of TaqMan assays for detection in this heterogenous species complex. Eur J Plant Pathol 2021; 159:593–613 [View Article]
    [Google Scholar]
  62. 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]
  63. Dia NC, Van Vaerenbergh J, Van Malderghem C, Blom J, Smits THM et al. Xanthomonas hydrangeae sp. nov., a novel plant pathogen isolated from Hydrangea arborescens. Int J Syst Evol Microbiol 2021; 71:005163 [View Article]
    [Google Scholar]
  64. Harrison J, Hussain RMF, Aspin A, Grant MR, Vicente JG et al. Phylogenomic analysis supports the transfer of 20 pathovars from Xanthomonas campestris into Xanthomonas euvesicatoria. Taxonomy 2023; 3:29–45 [View Article]
    [Google Scholar]
  65. Constantin EC, Cleenwerck I, Maes M, Baeyen S, 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]
  66. Walter Lack H. The discovery, naming and typification of Euphorbia pulcherrima (Euphorbiaceae). Willdenowia 2011; 41:301–309 [View Article]
    [Google Scholar]
  67. Li B, Yu R, Shi Y, Su T, Wang F et al. Reclassification of Xanthomonas isolates causing bacterial leaf spot of Euphorbia pulcherrima. Plant Pathol J 2011; 27:360–366 [View Article]
    [Google Scholar]
  68. Rockey W, Potnis N, Timilsina S, Hong JC, Vallad GE et al. Multilocus Sequence Analysis Reveals Genetic Diversity in Xanthomonads Associated With Poinsettia Production. Plant Dis 2015; 99:874–882 [View Article] [PubMed]
    [Google Scholar]
  69. Tambong JT, Xu R, Cuppels D, Chapados J, Gerdis S et al. Whole-genome resources and species-level taxonomic validation of 89 plant-pathogenic Xanthomonas strains isolated from various host plants. Plant Dis 2022; 106:1558–1565 [View Article] [PubMed]
    [Google Scholar]
  70. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article] [PubMed]
    [Google Scholar]
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