1887

Abstract

The economically important plant pathogen has been reported in multiple regions of the globe during the last two decades, threatening a growing list of plants. Particularly, subspecies causes Pierce’s disease (PD) of grapevines, which is a problem in the USA, Spain, and Taiwan. In this work, we studied PD-causing subsp. populations and compared the genome sequences of 33 isolates found in Central Taiwan with 171 isolates from the USA and two from Spain. Phylogenetic relationships, haplotype networks, and genetic diversity analyses confirmed that subsp. was recently introduced into Taiwan from the Southeast USA (i.e. the PD-I lineage). Recent core-genome recombination events were detected among introduced subsp. isolates in Taiwan and contributed to the development of genetic diversity. The genetic diversity observed includes contributions through recombination from unknown donors, suggesting that higher genetic diversity exists in the region. Nevertheless, no recombination event was detected between subsp. and the endemic sister species , which is the causative agent of pear leaf scorch disease. In summary, this study improved our understanding of the genetic diversity of an important plant pathogenic bacterium after its invasion to a new region.

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2021-12-13
2022-01-28
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References

  1. de Bruyn M, Stelbrink B, Morley RJ, Hall R, Carvalho GR et al. Borneo and Indochina are major evolutionary hotspots for Southeast Asian biodiversity. Syst Biol 2014; 63:879–901 [View Article] [PubMed]
    [Google Scholar]
  2. Hughes AC. Understanding the drivers of Southeast Asian biodiversity loss. Ecosphere 2017; 8:e01624 [View Article]
    [Google Scholar]
  3. Lohman DJ, de Bruyn M, Page T, von Rintelen K, Hall R et al. Biogeography of the Indo-Australian Archipelago. Annu Rev Ecol Evol Syst 2011; 42:205–226 [View Article]
    [Google Scholar]
  4. Sholihah A, Delrieu-Trottin E, Condamine FL, Wowor D, Rüber L et al. Impact of Pleistocene eustatic fluctuations on evolutionary dynamics in Southeast Asian biodiversity hotspots. Syst Biol 2021; 70:940–960 [View Article] [PubMed]
    [Google Scholar]
  5. Liao C-C, Chen C-H. Investigation of floristic similarities between Taiwan and terrestrial ecoregions in Asia using GBIF data. Bot Stud 2017; 58:15 [View Article] [PubMed]
    [Google Scholar]
  6. Hsieh C-F. Composition, endemism and phytogeographical affinities of the Taiwan flora. Taiwania 2002; 47:298–310
    [Google Scholar]
  7. Wu S-H, Hsieh C-F, Rejmánek M. Catalogue of the naturalized flora of Taiwan. Taiwania 2004; 49:16–31
    [Google Scholar]
  8. Yeh Y. Status and management of invasive species in Taiwan. Food and Fertilizer Technology Center. Food and Fertilizer Technology Center; 2005 https://www.fftc.org.tw/en/publications/main/439
  9. Wu ML. The threat of invasive alien pathogens to trees. For Res Newsl 2006; 13:15–17
    [Google Scholar]
  10. Martins PMM, Merfa MV, Takita MA, De Souza AA. Persistence in phytopathogenic bacteria: do we know enough?. Front Microbiol 2018; 9:1099. [View Article] [PubMed]
    [Google Scholar]
  11. Fones HN, Bebber DP, Chaloner TM, Kay WT, Steinberg G et al. Threats to global food security from emerging fungal and oomycete crop pathogens. Nat Food 2020; 1:332–342 [View Article]
    [Google Scholar]
  12. Avery SV, Singleton I, Magan N, Goldman GH. The fungal threat to global food security. Fungal Biol 2019; 123:555–557 [View Article] [PubMed]
    [Google Scholar]
  13. Bebber DP, Field E, Gui H, Mortimer P, Holmes T et al. Many unreported crop pests and pathogens are probably already present. Glob Change Biol 2019; 25:2703–2713 [View Article]
    [Google Scholar]
  14. Bebber DP, Gurr SJ. Crop-destroying fungal and oomycete pathogens challenge food security. Fungal Genet Biol 2015; 74:62–64 [View Article] [PubMed]
    [Google Scholar]
  15. Oerke E-C. Crop losses to pests. J Agric Sci 2005; 144:31–43 [View Article]
    [Google Scholar]
  16. Paini DR, Sheppard AW, Cook DC, De Barro PJ, Worner SP et al. Global threat to agriculture from invasive species. Proc Natl Acad Sci U S A 2016; 113:7575–7579 [View Article] [PubMed]
    [Google Scholar]
  17. Savary S, Bregaglio S, Willocquet L, Gustafson D, Mason D’Croz D et al. Crop health and its global impacts on the components of food security. Food Sec 2017; 9:311–327 [View Article]
    [Google Scholar]
  18. Savary S, Ficke A, Aubertot J-N, Hollier C. Crop losses due to diseases and their implications for global food production losses and food security. Food Sec 2012; 4:519–537 [View Article]
    [Google Scholar]
  19. Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N et al. The global burden of pathogens and pests on major food crops. Nat Ecol Evol 2019; 3:430–439 [View Article] [PubMed]
    [Google Scholar]
  20. Strange RN, Scott PR. Plant disease: A threat to global food security. Annu Rev Phytopathol 2005; 43:83–116 [View Article] [PubMed]
    [Google Scholar]
  21. He D, Zhan J, Xie L. Problems, challenges and future of plant disease management: from an ecological point of view. Journal of Integrative Agriculture 2016; 15:705–715 [View Article]
    [Google Scholar]
  22. Occhibove F, Chapman DS, Mastin AJ, Parnell SSR, Agstner B et al. Eco-epidemiological uncertainties of emerging plant diseases: The challenge of predicting Xylella fastidiosa dynamics in novel environments. Phytopathology 2020; 110:1740–1750 [View Article] [PubMed]
    [Google Scholar]
  23. Parnell S, van den Bosch F, Gottwald T, Gilligan CA. Surveillance to inform control of emerging plant diseases: an epidemiological perspective. Annu Rev Phytopathol 2017; 55:591–610 [View Article] [PubMed]
    [Google Scholar]
  24. McDonald BA, Stukenbrock EH. Rapid emergence of pathogens in agro-ecosystems: global threats to agricultural sustainability and food security. Phil Trans R Soc B 2016; 371:20160026 [View Article]
    [Google Scholar]
  25. Read AF. The evolution of virulence. Trends Microbiol 1994; 2:73–76 [View Article] [PubMed]
    [Google Scholar]
  26. Croll D, McDonald BA. The genetic basis of local adaptation for pathogenic fungi in agricultural ecosystems. Mol Ecol 2017; 26:2027–2040 [View Article] [PubMed]
    [Google Scholar]
  27. Giraud T, Gladieux P, Gavrilets S. Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 2010; 25:387–395 [View Article] [PubMed]
    [Google Scholar]
  28. Mhedbi-Hajri N, Hajri A, Boureau T, Darrasse A, Durand K et al. Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLOS ONE 2013; 8:e58474 [View Article] [PubMed]
    [Google Scholar]
  29. Dutta A, Hartmann FE, Francisco CS, McDonald BA, Croll D. Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments. ISME J 2021; 15:1402–1419 [View Article] [PubMed]
    [Google Scholar]
  30. Sicard A, Zeilinger AR, Vanhove M, Schartel TE, Beal DJ et al. Xylella fastidiosa: insights into an emerging plant pathogen. Annu Rev Phytopathol 2018; 56:181–202 [View Article] [PubMed]
    [Google Scholar]
  31. Chatterjee S, Almeida RPP, Lindow S. Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Annu Rev Phytopathol 2008; 46:243–271 [View Article] [PubMed]
    [Google Scholar]
  32. Rapicavoli J, Ingel B, Blanco-Ulate B, Cantu D, Roper C. Xylella fastidiosa: an examination of a re-emerging plant pathogen. Mol Plant Pathol 2018; 19:786–800 [View Article] [PubMed]
    [Google Scholar]
  33. Roper C, Castro C, Ingel B. Xylella fastidiosa: bacterial parasitism with hallmarks of commensalism. Curr Opin Plant Biol 2019; 50:140–147 [View Article] [PubMed]
    [Google Scholar]
  34. Castillo AI, Chacón-Díaz C, Rodríguez-Murillo N, Coletta-Filho HD, Almeida RPP. Impacts of local population history and ecology on the evolution of a globally dispersed pathogen. BMC Genomics 2020; 21:369 [View Article] [PubMed]
    [Google Scholar]
  35. Nunney L, Azad H, Stouthamer R. An experimental test of the host-plant range of nonrecombinant strains of North American Xylella fastidiosa subsp. multiplex. Phytopathology 2019; 109:294–300 [View Article] [PubMed]
    [Google Scholar]
  36. Vanhove M, Sicard A, Ezennia J, Leviten N, Almeida RPP. Population structure and adaptation of a bacterial pathogen in California grapevines. Environ Microbiol 2020; 22:2625–2638 [View Article] [PubMed]
    [Google Scholar]
  37. Nunney L, Yuan X, Bromley RE, Stouthamer R. Detecting genetic introgression: High levels of intersubspecific recombination found in Xylella fastidiosa in Brazil. Appl Environ Microbiol 2012; 78:4702–4714 [View Article] [PubMed]
    [Google Scholar]
  38. Nunney L, Hopkins DL, Morano LD, Russell SE, Stouthamer R. Intersubspecific recombination in Xylella fastidiosa strains native to the United States: Infection of novel hosts associated with an unsuccessful invasion. Appl Environ Microbiol 2014; 80:1159–1169 [View Article] [PubMed]
    [Google Scholar]
  39. Gomila M, Moralejo E, Busquets A, Segui G, Olmo D et al. Draft genome resources of two strains of Xylella fastidiosa XYL1732/17 and XYL2055/17 isolated from Mallorca vineyards. Phytopathology 2019; 109:222–224 [View Article] [PubMed]
    [Google Scholar]
  40. Landa BB, Castillo AI, Giampetruzzi A, Kahn A, Román-Écija M et al. Emergence of a plant pathogen in Europe associated with multiple intercontinental introductions. Appl Environ Microbiol 2020; 86:e01521-19 [View Article] [PubMed]
    [Google Scholar]
  41. Olmo D, Nieto A, Adrover F, Urbano A, Beidas O et al. First detection of Xylella fastidiosa infecting cherry (Prunus avium) and Polygala myrtifolia plants, in Mallorca Island, Spain. Plant Dis 2017; 101:1820 [View Article]
    [Google Scholar]
  42. Saponari M, Giampetruzzi A, Loconsole G, Boscia D, Saldarelli P. Xylella fastidiosa in olive in Apulia: Where we stand. Phytopathology 2019; 109:175–186 [View Article] [PubMed]
    [Google Scholar]
  43. Su C-C, Chang CJ, Chang C-M, Shih H-T, Tzeng K-C et al. Pierce’s disease of grapevines in Taiwan: Isolation, cultivation and pathogenicity of Xylella fastidiosa. J Phytopathol 2013; 161:389–396 [View Article]
    [Google Scholar]
  44. Castillo AI, Tuan S-J, Retchless AC, Hu F-T, Chang H-Y et al. Draft whole-genome sequences of Xylella fastidiosa subsp. fastidiosa strains TPD3 and TPD4, isolated from grapevines in Hou-li, Taiwan. Microbiol Resour Announc 2019; 8:e00835-19 [View Article] [PubMed]
    [Google Scholar]
  45. Castillo AI, Bojanini I, Chen H, Kandel PP, De La Fuente L et al. Allopatric plant pathogen population divergence following disease emergence. Appl Environ Microbiol 2021; 87:e02095-20 [View Article] [PubMed]
    [Google Scholar]
  46. Lin YS, Chang YL. The insect vectors of Pierce’s disease on grapevines in Taiwan. Formos Entomol 2012; 32:155–167
    [Google Scholar]
  47. Tuan S-J, Hu F-T, Chang H-Y, Chang P-W, Chen Y-H et al. Xylella fastidiosa transmission and life history of two Cicadellinae sharpshooters, Kolla paulula and Bothrogonia ferruginea (Hemiptera: Cicadellidae), in Taiwan. J Econ Entomol 2016; 109:1034–1040 [View Article] [PubMed]
    [Google Scholar]
  48. Su C-C, Chang C-M, Chang C-J, Su W-Y, Chu J-C et al. Occurrence of Pierce’s disease of grapevines and its control strategies in Taiwan. Plant Pathol Bull 2013; 22:245–258
    [Google Scholar]
  49. Wistrom C, Purcell AH. The fate of Xylella fastidiosa in vineyard weeds and other alternate hosts in California. Plant Dis 2005; 89:994–999 [View Article] [PubMed]
    [Google Scholar]
  50. Leu L-S, Su C-C. Isolation, cultivation, and pathogenicity of Xylella fastidiosa, the causal bacterium of pear leaf scorch disease in Taiwan. Plant Dis 1993; 77:642-646 [View Article]
    [Google Scholar]
  51. Su C-C, Deng W-L, Jan F-J, Chang C-J, Huang H et al. Draft genome sequence of Xylella fastidiosa pear leaf scorch strain in Taiwan. Genome Announc 2014; 2:e00166-14 [View Article]
    [Google Scholar]
  52. Su C-C, Deng W-L, Jan F-J, Chang C-J, Huang H et al. Xylella taiwanensis sp. nov., causing pear leaf scorch disease. Int J Syst Evol Microbiol 2016; 66:4766–4771 [View Article] [PubMed]
    [Google Scholar]
  53. Weng L-W, Lin Y-C, Su C-C, Huang C-T, Cho S-T et al. Complete genome sequence of Xylella taiwanensis and comparative analysis of virulence gene content with Xylella fastidiosa. Front Microbiol 2021; 12:684092. [View Article] [PubMed]
    [Google Scholar]
  54. 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]
  55. Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  56. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 2018; 34:3094–3100 [View Article] [PubMed]
    [Google Scholar]
  57. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  58. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES et al. Integrative genomics viewer. Nat Biotechnol 2011; 29:24–26 [View Article] [PubMed]
    [Google Scholar]
  59. 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]
  60. Wingett SW, Andrews S. FastQ screen: A tool for multi-genome mapping and quality control. F1000Res 2018; 7:1338 [View Article] [PubMed]
    [Google Scholar]
  61. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 2011; 17:10 [View Article]
    [Google Scholar]
  62. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  63. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [View Article] [PubMed]
    [Google Scholar]
  64. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD et al. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 2009; 25:2071–2073 [View Article] [PubMed]
    [Google Scholar]
  65. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  66. Scally M, Schuenzel EL, Stouthamer R, Nunney L. Multilocus sequence type system for the plant pathogen Xylella fastidiosa and relative contributions of recombination and point mutation to clonal diversity. Appl Environ Microbiol 2005; 71:8491–8499 [View Article] [PubMed]
    [Google Scholar]
  67. Yuan X, Morano L, Bromley R, Spring-Pearson S, Stouthamer R et al. Multilocus sequence typing of Xylella fastidiosa causing Pierce’s disease and oleander leaf scorch in the United States. Phytopathology 2010; 100:601–611 [View Article] [PubMed]
    [Google Scholar]
  68. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  69. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  70. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article] [PubMed]
    [Google Scholar]
  71. Mostowy R, Croucher NJ, Andam CP, Corander J, Hanage WP et al. Efficient inference of recent and ancestral recombination within bacterial populations. Mol Biol Evol 2017; 34:1167–1182 [View Article] [PubMed]
    [Google Scholar]
  72. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  73. Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ. PopGenome: An efficient Swiss Army knife for population genomic analyses in R. Mol Biol Evol 2014; 31:1929–1936 [View Article] [PubMed]
    [Google Scholar]
  74. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123:585–595 [View Article] [PubMed]
    [Google Scholar]
  75. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol 1975; 7:256–276 [View Article] [PubMed]
    [Google Scholar]
  76. Paradis E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 2010; 26:419–420 [View Article] [PubMed]
    [Google Scholar]
  77. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microbial Genomics 2016; 2:e000056 [View Article]
    [Google Scholar]
  78. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. RhierBAPS: An R implementation of the population clustering algorithm hierBAPS. Wellcome Open Res 2018; 3:93 [View Article] [PubMed]
    [Google Scholar]
  79. LeBlanc N, Cubeta MA, Crouch JA. Population genomics trace clonal diversification and intercontinental migration of an emerging fungal pathogen of boxwood. Phytopathology 2021; 111:184–193 [View Article] [PubMed]
    [Google Scholar]
  80. Moralejo E, Gomila M, Montesinos M, Borràs D, Pascual A et al. Phylogenetic inference enables reconstruction of a long-overlooked outbreak of almond leaf scorch disease (Xylella fastidiosa) in Europe. Commun Biol 2020; 3:560 [View Article] [PubMed]
    [Google Scholar]
  81. Soubeyrand S, de Jerphanion P, Martin O, Saussac M, Manceau C et al. Inferring pathogen dynamics from temporal count data: the emergence of Xylella fastidiosa in France is probably not recent. New Phytol 2018; 219:824–836 [View Article] [PubMed]
    [Google Scholar]
  82. Vieira A, Silva DN, Várzea V, Paulo OS, Batista D. Novel insights on colonization routes and evolutionary potential of Colletotrichum kahawae, a severe pathogen of Coffea arabica. Mol Plant Pathol 2018; 19:2488–2501 [View Article] [PubMed]
    [Google Scholar]
  83. Robert S, Ravigne V, Zapater M-F, Abadie C, Carlier J. Contrasting introduction scenarios among continents in the worldwide invasion of the banana fungal pathogen Mycosphaerella fijiensis. Mol Ecol 2012; 21:1098–1114 [View Article] [PubMed]
    [Google Scholar]
  84. Giampetruzzi A, Saponari M, Loconsole G, Boscia D, Savino VN et al. Genome-wide analysis provides evidence on the genetic relatedness of the emergent Xylella fastidiosa genotype in Italy to isolates from Central America. Phytopathology 2017; 107:816–827 [View Article] [PubMed]
    [Google Scholar]
  85. Nunney L, Ortiz B, Russell SA, Ruiz Sánchez R, Stouthamer R. The complex biogeography of the plant pathogen Xylella fastidiosa: Genetic evidence of introductions and subspecific introgression in Central America. PLOS ONE 2014; 9:e112463 [View Article] [PubMed]
    [Google Scholar]
  86. Nunney L, Schuenzel EL, Scally M, Bromley RE, Stouthamer R. Large-scale intersubspecific recombination in the plant-pathogenic bacterium Xylella fastidiosa is associated with the host shift to mulberry. Appl Environ Microbiol 2014; 80:3025–3033 [View Article] [PubMed]
    [Google Scholar]
  87. Nunney L, Vickerman DB, Bromley RE, Russell SA, Hartman JR et al. Recent evolutionary radiation and host plant specialization in the Xylella fastidiosa subspecies native to the United States. Appl Environ Microbiol 2013; 79:2189–2200 [View Article] [PubMed]
    [Google Scholar]
  88. Nunney L, Yuan X, Bromley R, Hartung J, Montero-Astúa M et al. Population genomic analysis of a bacterial plant pathogen: novel insight into the origin of Pierce’s disease of grapevine in the U.S. PLOS ONE 2010; 5:e15488 [View Article] [PubMed]
    [Google Scholar]
  89. Iranzo J, Wolf YI, Koonin EV, Sela I. Gene gain and loss push prokaryotes beyond the homologous recombination barrier and accelerate genome sequence divergence. Nat Commun 2019; 10:5376. [View Article] [PubMed]
    [Google Scholar]
  90. Vanhove M, Retchless AC, Sicard A, Rieux A, Coletta-Filho HD et al. Genomic diversity and recombination among Xylella fastidiosa subspecies. Appl Environ Microbiol 2019; 85:e02972-18 [View Article] [PubMed]
    [Google Scholar]
  91. Almeida RPP, Nascimento FE, Chau J, Prado SS, Tsai C-W et al. Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil. Appl Environ Microbiol 2008; 74:3690–3701 [View Article] [PubMed]
    [Google Scholar]
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