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Abstract

Many bacterial pathogens are well characterized but, in some cases, little is known about the populations from which they emerged. This limits understanding of the molecular mechanisms underlying disease. The crop pathogen Pseudomonas syringae sensu lato has been widely isolated from the environment, including wild plants and components of the water cycle, and causes disease in several economically important crops. Here, we compared genome sequences of 45 P. syringae crop pathogen outbreak strains with 69 closely related environmental isolates. Phylogenetic reconstruction revealed that crop pathogens emerged many times independently from environmental populations. Unexpectedly, differences in gene content between environmental populations and outbreak strains were minimal with most virulence genes present in both. However, a genome-wide association study identified a small number of genes, including the type III effector genes hopQ1 and hopD1, to be associated with crop pathogens, but not with environmental populations, suggesting that this small group of genes may play an important role in crop disease emergence. Intriguingly, genome-wide analysis of homologous recombination revealed that the locus Psyr 0346, predicted to encode a protein that confers antibiotic resistance, has been frequently exchanged among lineages and thus may contribute to pathogen fitness. Finally, we found that isolates from diseased crops and from components of the water cycle, collected during the same crop disease epidemic, form a single population. This provides the strongest evidence yet that precipitation and irrigation water are an overlooked inoculum source for disease epidemics caused by P. syringae.

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2016-10-01
2024-12-07
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References

  1. Alfano J. R., Collmer A. 2004; Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annual Review of . Phytopathology 42:385–414
    [Google Scholar]
  2. Andrews S. 2010; FastQC: A quality control tool for high throughput sequence data. Bioinformatics http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
    [Google Scholar]
  3. Bartoli C., Lamichhane J. R., Berge O., Guilbaud C., Varvaro L., Balestra G. M., Vinatzer B. A., Morris C. E. 2015; A framework to gauge the epidemic potential of plant pathogens in environmental reservoirs: the example of kiwifruit canker. Mol Plant Pathol 16:137–149 [View Article][PubMed]
    [Google Scholar]
  4. Berge O., Monteil C. L., Bartoli C., Chandeysson C., Guilbaud C., Sands D. C., Morris C. E. 2014; A user's guide to a data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLoS One 9:e105547 [View Article][PubMed]
    [Google Scholar]
  5. Block A., Toruño T. Y., Elowsky C. G., Zhang C., Steinbrenner J., Beynon J., Alfano J. R. 2014; The Pseudomonas syringae type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9. New Phytol 201:1358–1370 [View Article][PubMed]
    [Google Scholar]
  6. Buell C. R., Joardar V., Lindeberg M., Selengut J., Paulsen I. T., Gwinn M. L., Dodson R. J., Deboy R. T., Durkin A. S. et al. 2003; The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 100:10181–10186 [View Article][PubMed]
    [Google Scholar]
  7. Cai R., Lewis J., Yan S., Liu H., Clarke C. R., Campanile F., Almeida N. F., Studholme D. J., Lindeberg M. et al. 2011a; The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathogens 7:e1002130 [View Article]
    [Google Scholar]
  8. Cai R., Yan S., Liu H., Leman S., Vinatzer B. A. 2011b; Reconstructing host range evolution of bacterial plant pathogens using Pseudomonas syringae pv. tomato and its close relatives as a model. Infection Genetics and . Evolution 11:1738–1751
    [Google Scholar]
  9. Carver T., Thomson N., Bleasby A., Berriman M., Parkhill J. 2009; DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25:119–120 [View Article][PubMed]
    [Google Scholar]
  10. Chen X. M. 2005; Epidemiology and control of stripe rust Puccinia striiformis f. sp tritici on wheat. Canadian Journal of Plant Pathology 27:314–337
    [Google Scholar]
  11. Cheng L., Connor T. R., Siren J., Aanensen D. M., Corander J. 2013; Hierarchical and Spatially Explicit Clustering of DNA Sequences with BAPS Software. Molecular Biology and . Evolution 30:1224–1228
    [Google Scholar]
  12. Clarke C. R., Studholme D. J., Hayes B., Runde B., Weisberg A., Cai R., Wroblewski T., Daunay M. C., Wicker E. et al. 2015; Genome-enabled phylogeographic investigation of the quarantine pathogen Ralstonia solanacearum race 3 biovar 2 and screening for sources of resistance against its core effectors. Phytopathology 105:597–607 [View Article][PubMed]
    [Google Scholar]
  13. Constantinidou H. A., Hirano S. S., Baker L. S., Upper C. D. 1990; Atmospheric dispersal of ice nucleation-active bacteria: the role of rain. Phytopathology 80:934–937 [View Article]
    [Google Scholar]
  14. Corander J., Waldmann P., Marttinen P., Sillanpää M. J. 2004; BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20:2363–2369 [View Article][PubMed]
    [Google Scholar]
  15. Corander J., Marttinen P., Sirén J., Tang J. 2008; Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9: [View Article][PubMed]
    [Google Scholar]
  16. Demba Diallo M., Monteil C. L., Vinatzer B. A., Clarke C. R., Glaux C., Guilbaud C., Desbiez C., Morris C. E. 2012; Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic. ISME J 6:1325–1335 [View Article][PubMed]
    [Google Scholar]
  17. Didelot X., Falush D. 2007; Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266 [View Article][PubMed]
    [Google Scholar]
  18. Feil H., Feil W. S., Chain P., Larimer F., DiBartolo G., Copeland A., Lykidis A., Trong S., Nolan M. et al. 2005; Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A 102:11064–11069 [View Article][PubMed]
    [Google Scholar]
  19. Garland T., Bennett A. F., Rezende E. L. 2005; Phylogenetic approaches in comparative physiology. J Exp Biol 208:3015–3035 [View Article][PubMed]
    [Google Scholar]
  20. Gitaitis R., Walcott R. 2007; The epidemiology and management of seedborne bacterial diseases. Annu Rev Phytopathol 45:371–397 [View Article][PubMed]
    [Google Scholar]
  21. Grosso-Becerra M. V., Santos-Medellín C., González-Valdez A., Méndez J. L., Delgado G., Morales-Espinosa R., Servín-González L., Alcaraz L. D., Soberón-Chávez G. 2014; Pseudomonas aeruginosa clinical and environmental isolates constitute a single population with high phenotypic diversity. BMC Genomics 15: [View Article][PubMed]
    [Google Scholar]
  22. Hanage W. P., Fraser C., Tang J., Connor T. R., Corander J. 2009; Hyper-recombination, diversity, and antibiotic resistance in pneumococcus. Science 324:1454–1457 [View Article][PubMed]
    [Google Scholar]
  23. Hann D. R., Domínguez-Ferreras A., Motyka V., Dobrev P., Schornack S., Jehle A., Felix G., Chinchilla D., Rathjen J. P., Boller T. 2014; The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol 201:585–598 [View Article][PubMed]
    [Google Scholar]
  24. Hazen T. H., Lafon P. C., Garrett N. M., Lowe T. M., Silberger D. J., Rowe L. A., Frace M., Parsons M. B., Bopp C. A. et al. 2015; Insights into the environmental reservoir of pathogenic Vibrio parahaemolyticus using comparative genomics. Front Microbiol 6:204 [View Article][PubMed]
    [Google Scholar]
  25. Hirano S. S., Upper C. D. 2000; Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64:624–653 [View Article][PubMed]
    [Google Scholar]
  26. Hockett K. L., Nishmura M., Karsrud E., Dougherty K. M., Baltrus D. A. 2014; P. syringae CC1557: a highly virulent strain with an unusually small type III effector repertoire that includes a novel effector. Am Phytopath Society
    [Google Scholar]
  27. Joardar V., Lindeberg M., Jackson R. W., Selengut J., Dodson R., Brinkac L. M., Daugherty S. C., Deboy R., Durkin A. S. et al. 2005; Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J Bacteriol 187:6488–6498 [View Article][PubMed]
    [Google Scholar]
  28. Johnson P. T., de Roode J. C., Fenton A. 2015; Why infectious disease research needs community ecology. Science 349: [View Article][PubMed]
    [Google Scholar]
  29. Jolley K. A., Maiden M. C. 2010; BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: [View Article][PubMed]
    [Google Scholar]
  30. Katoh K., Toh H. 2008; Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298 [View Article][PubMed]
    [Google Scholar]
  31. Krueger F. 2015; Trim Galore!: A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files. http://www.bioinformatics.babraham.ac.uk/projects/trim_galore/
  32. Lawson D. J., Hellenthal G., Myers S., Falush D. 2012; Inference of population structure using dense haplotype data. PLoS Genet 8: [View Article][PubMed]
    [Google Scholar]
  33. Li W., Chiang Y.-H., Coaker G. 2013a; The HopQ1 effector’s nucleoside hydrolase-like domain is required for bacterial virulence in arabidopsis and tomato, but not host recognition in Tobacco. PLoS ONE 8:e59684 [View Article]
    [Google Scholar]
  34. Li W., Yadeta K. A., Elmore J. M., Coaker G. 2013; The Pseudomonas syringae Effector HopQ1 Promotes Bacterial Virulence and Interacts with Tomato 14-3-3 Proteins in a Phosphorylation-Dependent Manner. PLANT PHYSIOLOGY 161:2062–2074 [View Article]
    [Google Scholar]
  35. Lindeberg M., Myers C. R., Collmer A., Schneider D. J. 2008; Roadmap to new virulence determinants in Pseudomonas syringae: Insights from comparative genomics and genome organization. Mol Plant Microbe In 21:685–700
    [Google Scholar]
  36. Maiden M. C., Jansen van Rensburg M. J., Bray J. E., Earle S. G., Ford S. A., Jolley K. A., McCarthy N. D. 2013; MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11:728–736 [View Article][PubMed]
    [Google Scholar]
  37. Martin M. 2011; Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17:10 [View Article]
    [Google Scholar]
  38. Martins E. P., Garland T. 1991; Phylogenetic analyses of the correlated evolution of continuous characters: a simulation study. Evolution 45:534–557 [View Article]
    [Google Scholar]
  39. McCann H. C., Rikkerink E. H., Bertels F., Fiers M., Lu A., Rees-George J., Andersen M. T., Gleave A. P., Haubold B. et al. 2013; Genomic analysis of the Kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease. PLoS Pathog 9:e1003503 [View Article][PubMed]
    [Google Scholar]
  40. McCarter S. M., Jones J. B., Gitaitis R. D., Smitley D. R. 1983; Survival of Pseudomonas syringae pv. tomato in association with tomato seed, soil, host tissue, and epiphytic weed hosts in Georgia. Phytopathology 73:1393–1398 [View Article]
    [Google Scholar]
  41. Méric G., Yahara K., Mageiros L., Pascoe B., Maiden M. C., Jolley K. A., Sheppard S. K. 2014; A reference pan-genome approach to comparative bacterial genomics: identification of novel epidemiological markers in pathogenic Campylobacter . PLoS One 9:e92798 [View Article][PubMed]
    [Google Scholar]
  42. Mohr T. J., Liu H., Yan S., Morris C. E., Castillo J. A., Jelenska J., Vinatzer B. A. 2008; Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues. J Bacteriol 190:2858–2870 [View Article][PubMed]
    [Google Scholar]
  43. Monteil C. L., Guilbaud C., Glaux C., Lafolie F., Soubeyrand S., Morris C. E. 2012; Emigration of the plant pathogen Pseudomonas syringae from leaf litter contributes to its population dynamics in alpine snowpack. Environ Microbiol 14:2099–2112 [View Article][PubMed]
    [Google Scholar]
  44. Monteil C. L., Cai R., Liu H., Llontop M. E., Leman S., Studholme D. J., Morris C. E., Vinatzer B. A. 2013; Nonagricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens. New Phytol 199:800–811 [View Article][PubMed]
    [Google Scholar]
  45. Monteil C. L., Bardin M., Morris C. E. 2014a; Features of air masses associated with the deposition of Pseudomonas syringae and Botrytis cinerea by rain and snowfall. ISME J 8:2290–2304 [View Article]
    [Google Scholar]
  46. Monteil C. L., Lafolie F., Laurent J., Clement J. C., Simler R., Travi Y., Morris C. E. 2014b; Soil water flow is a source of the plant pathogen Pseudomonas syringae in subalpine headwaters. Environ Microbiol 16:2038–2052 [View Article][PubMed]
    [Google Scholar]
  47. Morris C. E., Glaux C., Latour X., Gardan L., Samson R., Pitrat M. 2000; The Relationship of host range, physiology, and genotype to virulence on cantaloupe in pseudomonas syringae from cantaloupe blight epidemics in France. Phytopathology 90:636–646 [View Article][PubMed]
    [Google Scholar]
  48. Morris C. E., Sands D. C., Vinatzer B. A., Glaux C., Guilbaud C., Buffière A., Yan S., Dominguez H., Thompson B. M. 2008; The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2:321–334 [View Article][PubMed]
    [Google Scholar]
  49. Morris C. E., Sands D. C., Vanneste J. L., Montarry J., Oakley B., Guilbaud C., Glaux C. 2010; Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. MBio 1:e00107-10e00107-20 [View Article][PubMed]
    [Google Scholar]
  50. Morris C. E., Monteil C. L., Berge O. 2013; The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu Rev Phytopathol 51:85–104 [View Article][PubMed]
    [Google Scholar]
  51. O'Brien H. E., Thakur S., Guttman D. S. 2011; Evolution of plant pathogenesis in Pseudomonas syringae: a genomics perspective. Annu Rev Phytopathol 49:269–289 [View Article][PubMed]
    [Google Scholar]
  52. Ochman H., Lawrence J. G., Groisman E. A. 2000; Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 [View Article][PubMed]
    [Google Scholar]
  53. Pascoe B., Meric G., Murray S., Mageiros L., Yahara K., Bowen R., Jones N. H., Jeeves R. E., Lappin-Scott H. M. et al. 2015; Enhanced biofilm formation evolves from divergent genetic backgrounds in host generalist Campylobacter jejuni . Environ Microbiol 17:4779–4789
    [Google Scholar]
  54. Piddock L. 2006; Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4:629–636 [View Article][PubMed]
    [Google Scholar]
  55. Price M. N., Dehal P. S., Arkin A. P. 2010; FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490 [View Article][PubMed]
    [Google Scholar]
  56. Rutherford K., Parkhill J., Crook J., Horsnell T., Rice P., Rajandream M. A., Barrell B. 2000; Artemis: sequence visualization and annotation. Bioinformatics 16:944–945 [View Article][PubMed]
    [Google Scholar]
  57. Sheppard S. K., Jolley K. A., Maiden M. C. 2012; A Gene-By-Gene Approach to Bacterial Population Genomics: Whole Genome MLST of Campylobacter . Genes 3:261–277 [View Article][PubMed]
    [Google Scholar]
  58. Sheppard S. K., Didelot X., Meric G., Torralbo A., Jolley K. A., Kelly D. J., Bentley S. D., Maiden M. C., Parkhill J., Falush D. 2013; Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter . Proc Natl Acad Sci U S A 110:11923–11927 [View Article][PubMed]
    [Google Scholar]
  59. Singh R. P., Hodson D. P., Huerta-Espino J., Jin Y., Bhavani S., Njau P., Herrera-Foessel S., Singh P. K., Singh S., Govindan V. 2011; The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481 [View Article][PubMed]
    [Google Scholar]
  60. Struve C., Krogfelt K. A. 2004; Pathogenic potential of environmental Klebsiella pneumoniae isolates. Environ Microbiol 6:584–590 [View Article][PubMed]
    [Google Scholar]
  61. Stukenbrock E. H., McDonald B. A. 2008; The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100 [View Article][PubMed]
    [Google Scholar]
  62. Tampakaki A. P., Skandalis N., Gazi A. D., Bastaki M. N., Sarris P. F., Charova S. N., Kokkinidis M., Panopoulos N. J. 2011; Playing the “Harp”: evolution of our understanding of hrp/hrc genes. Annu Rev Phytopathol 48:347–370
    [Google Scholar]
  63. Vinatzer B. A., Monteil C. L., Clarke C. R. 2014; Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu Rev Phytopathol 52,:19–43 [View Article][PubMed]
    [Google Scholar]
  64. Wei C. F., Kvitko B. H., Shimizu R., Crabill E., Alfano J. R., Lin N. C., Martin G. B., Huang H. C., Collmer A. 2007; A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana . Plant J 51:32–46 [View Article][PubMed]
    [Google Scholar]
  65. Whiley H., van den Akker B., Giglio S., Bentham R. 2013; The role of environmental reservoirs in human campylobacteriosis. Int J Environ Res Public Health 10:5886–5907 [View Article][PubMed]
    [Google Scholar]
  66. Woolhouse M. E., Taylor L. H., Haydon D. T. 2001; Population biology of multihost pathogens. Science 292:1109–1112 [View Article][PubMed]
    [Google Scholar]
  67. Xin X. F., He S. Y. 2013; Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 51:473–498 [View Article][PubMed]
    [Google Scholar]
  68. Yahara K., Furuta Y., Oshima K., Yoshida M., Azuma T., Hattori M., Uchiyama I., Kobayashi I. 2013; Chromosome painting in silico in a bacterial species reveals fine population structure. Molecular Biology and . Evolution 30:1454–1464
    [Google Scholar]
  69. Yahara K., Didelot X., Ansari M. A., Sheppard S. K., Falush D. 2014; Efficient inference of recombination hot regions in bacterial genomes. Mol Biol Evol 31:1593–1605 [View Article][PubMed]
    [Google Scholar]
  70. Yahara K., Didelot X., Jolley K. A., Kobayashi I., Maiden M. C., Sheppard S. K., Falush D. 2016a; The landscape of realized homologous recombination in pathogenic bacteria. Mol Biol Evol 33:456–471 [View Article][PubMed]
    [Google Scholar]
  71. Yahara K., Taylor A., de Vries S., Murray S., Pascoe B., Mageiros L., Torralbo A., Vidal A., Ridley A. et al. 2016b; Genome-wide association of functional traits linked with Campylobacter jejuni survival from farm to fork. PeerJ Preprints 4:e2300v1
    [Google Scholar]
  72. Yan S., Liu H., Mohr T. J., Jenrette J., Chiodini R., Zaccardelli M., Setubal J. C., Vinatzer B. A. 2008; Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Applied and Environmental . Microbiology 74:3171–3181
    [Google Scholar]
  73. Zerbino D. R., Birney E. 2008; Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829 [View Article][PubMed]
    [Google Scholar]
  74. Studholme, D., Monteil C., Swingle B. and Vinatzer, B. A. NCBI, Pseudomonas syringae BioProject (ID 320409) 2016
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