Crop diseases emerge without warning. In many cases, diseases cross borders, or even oceans, before plant pathologists have time to identify and characterize the causative agents. Genome sequencing, in combination with intensive sampling of pathogen populations and application of population genetic tools, is now providing the means to unravel how bacterial crop pathogens emerge from environmental reservoirs, how they evolve and adapt to crops, and what international and intercontinental routes they follow during dissemination. Here, we introduce the field of population genomics and review the population genomics research of bacterial plant pathogens over the past 10 years. We highlight the potential of population genomics for investigating plant pathogens, using examples of population genomics studies of human pathogens. We also describe the complementary nature of the fields of population genomics and molecular plant-microbe interactions and propose how to translate new insights into improved disease prevention and control.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Achtman M, Wain J, Weill F-X, Nair S, Zhou Z. 1.  et al. 2012. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 8:e1002776 [Google Scholar]
  2. Ah-You N, Gagnevin L, Grimont PA, Brisse S, Nesme X. 2.  et al. 2009. Polyphasic characterization of xanthomonads pathogenic to members of the Anacardiaceae and their relatedness to species of Xanthomonas. Int. J. Syst. Evol. Microbiol. 59:306–18 [Google Scholar]
  3. Almeida NF, Yan S, Cai R, Clarke CR, Morris CE. 3.  et al. 2010. PAMDB, a multilocus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 100:208–15 [Google Scholar]
  4. Almeida RP, Nascimento FE, Chau J, Prado SS, Tsai CW. 4.  et al. 2008. Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil. Appl. Environ. Microbiol. 74:3690–701 [Google Scholar]
  5. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SLR, Cookson BT. 5.  et al. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA 102:9247–52 [Google Scholar]
  6. Arnold DL, Jackson RW, Waterfield NR, Mansfield JW. 6.  2007. Evolution of microbial virulence: the benefits of stress. Trends Genet. 23:293–300 [Google Scholar]
  7. Ausubel FM. 7.  2005. Are innate immune signaling pathways in plants and animals conserved?. Nat. Immunol. 6:973–79 [Google Scholar]
  8. Badel JL, Shimizu R, Oh H-S, Collmer A. 8.  2006. A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol. Plant-Microbe Interact. 19:99–111 [Google Scholar]
  9. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Shahid Mukhtar M. 9.  et al. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog. 7:e1002132 [Google Scholar]
  10. Bart R, Cohn M, Kassen A, McCallum EJ, Shybut M. 10.  et al. 2012. High-throughput genomic sequencing of cassava bacterial blight strains identifies conserved effectors to target for durable resistance. Proc. Natl. Acad. Sci. USA 109:E1972–79 [Google Scholar]
  11. Basim H, Stall RE, Minsavage GV, Jones JB. 11.  1999. Chromosomal gene transfer by conjugation in the plant pathogen Xanthomonas axonopodis pv. vesicatoria. Phytopathology 89:1044–49 [Google Scholar]
  12. Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV. 12.  et al. 2011. Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J. Bacteriol. 193:5450–64 [Google Scholar]
  13. Boller T, He SY. 13.  2009. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–44 [Google Scholar]
  14. Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T. 14.  2008. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst. Appl. Microbiol. 31:447–60 [Google Scholar]
  15. Brady CL, Venter SN, Cleenwerck I, Engelbeen K, Vancanneyt M. 15.  et al. 2009. Pantoea vagans sp. nov., Pantoea eucalypti sp. nov., Pantoea deleyi sp. nov. and Pantoea anthophila sp. nov. Int. J. Syst. Evol. Microbiol. 59:2339–45 [Google Scholar]
  16. Buhlmann A, Dreo T, Rezzonico F, Pothier JF, Smits TH. 16.  et al. 2014. Phylogeography and population structure of the biologically invasive phytopathogen Erwinia amylovora inferred using minisatellites. Environ. Microbiol. doi: 10.1111/1462-2920.12289
  17. Bui Thi Ngoc L, Verniere C, Jouen E, Ah-You N, Lefeuvre P. 17.  et al. 2010. Amplified fragment length polymorphism and multilocus sequence analysis-based genotypic relatedness among pathogenic variants of Xanthomonas citri pv. citri and Xanthomonas campestris pv. bilvae. Int. J. Syst. Evol. Microbiol. 60:515–25 [Google Scholar]
  18. Bull CT, Clarke CR, Cai R, Vinatzer BA, Jardini TM, Koike ST. 18.  2011. Multilocus sequence typing of Pseudomonas syringae sensu lato confirms previously described genomospecies and permits rapid identification of P. syringae pv. coriandricola and P. syringae pv. apii causing bacterial leaf spot on parsley. Phytopathology 101:847–58 [Google Scholar]
  19. Butler MI, Stockwell PA, Black MA, Day RC, Lamont IL, Poulter RTM. 19.  2013. Pseudomonas syringae pv. actinidiae from recent outbreaks of kiwifruit bacterial canker belong to different clones that originated in china. PLoS ONE 8:e57465 [Google Scholar]
  20. Cai R, Lewis J, Yan S, Liu H, Clarke CR. 20.  et al. 2011. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 7:e1002130 [Google Scholar]
  21. Cai R, Yan S, Liu H, Leman S, Vinatzer BA. 21.  2011. Reconstructing host range evolution of bacterial plant pathogens using Pseudomonas syringae pv. tomato and its close relatives as a model. Infect. Genet. Evol. 11:1738–51 [Google Scholar]
  22. Castillo JA, Greenberg JT. 22.  2007. Evolutionary dynamics of Ralstonia solanacearum. Appl. Environ. Microbiol. 73:1225–38 [Google Scholar]
  23. Che F-S, Nakajima Y, Tanaka N, Iwano M, Yoshida T. 23.  et al. 2000. Flagellin from an incompatible strain of Pseudomonas avenae induces a resistance response in cultured rice cells. J. Biol. Chem. 275:32347–56 [Google Scholar]
  24. Chisholm ST, Coaker G, Day B, Staskawicz BJ. 24.  2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–14 [Google Scholar]
  25. Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA. 25.  2010. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol. Plant-Microbe Interact. 23:198–210 [Google Scholar]
  26. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki Y. 26.  et al. 2013. Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol. 200:847–60 [Google Scholar]
  27. Coupat-Goutaland B, Bernillon D, Guidot A, Prior P, Nesme X, Bertolla F. 27.  2010. Ralstonia solanacearum virulence increased following large interstrain gene transfers by natural transformation. Mol. Plant-Microbe Interact. 24:497–505 [Google Scholar]
  28. Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM. 28.  et al. 2013. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat. Genet. 45:656–63 [Google Scholar]
  29. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J. 29.  et al. 2011. Rapid pneumococcal evolution in response to clinical interventions. Science 331:430–44 [Google Scholar]
  30. Cui Y, Yu C, Yan Y, Li D, Li Y. 30.  et al. 2013. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl. Acad. Sci. USA 110:577–82 [Google Scholar]
  31. da Silva ACR, Ferro JA, Reinach FC, Farah CS, Furlan LR. 31.  et al. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–63 [Google Scholar]
  32. Danet JL, Balakishiyeva G, Cimerman A, Sauvion N, Marie-Jeanne V. 32.  et al. 2011. Multilocus sequence analysis reveals the genetic diversity of European fruit tree phytoplasmas and supports the existence of inter-species recombination. Microbiology 157:438–50 [Google Scholar]
  33. Dangl JL, Horvath DM, Staskawicz BJ. 33.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  34. Davis RE, Zhao Y, Dally EL, Lee I-M, Jomantiene R, Douglas SM. 34.  2013. Candidatus Phytoplasma pruni,” a novel taxon associated with X-disease of stone fruits, Prunus spp.: multilocus characterization based on 16S rRNA, secY, and ribosomal protein genes. Int. J. Syst. Evol. Microbiol. 63:766–76 [Google Scholar]
  35. DebRoy S, Thilmony R, Kwack Y-B, Nomura K, He SY. 35.  2004. A family of conserved bacterial effectors inhibits salicylic acid–mediated basal immunity and promotes disease necrosis in plants. Proc. Natl. Acad. Sci. USA 101:9927–32 [Google Scholar]
  36. Deletoile A, Decre D, Courant S, Passet V, Audo J. 36.  et al. 2009. Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing. J. Clin. Microbiol. 47:300–10 [Google Scholar]
  37. Diallo MD, Monteil CL, Vinatzer BA, Clarke CR, Glaux C. 37.  et al. 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. 6:1325–35 [Google Scholar]
  38. Didelot X, Bowden R, Wilson DJ, Peto TEA, Crook DW. 38.  2012. Transforming clinical microbiology with bacterial genome sequencing. Nat. Rev. Genet. 13:601–12 [Google Scholar]
  39. Didelot X, Maiden MCJ. 39.  2010. Impact of recombination on bacterial evolution. Trends Microbiol. 18:315–22 [Google Scholar]
  40. Dye DW, Bradbury JF, Goto M, Hayward AC, Lelliott RA, Schroth MN. 40.  1980. International standards for naming pathovars of phytopathogenic bacteria and a list of pathovar names and pathotype strains. Rev. Plant Pathol. 59:153–68 [Google Scholar]
  41. Dykhuizen D, Kalia A. 41.  2007. The population structure of pathogenic bacteria. Evolution in Health and Disease SC Stearns, JC Koella 185–98 Oxford, UK: Oxford Univ. Press. [Google Scholar]
  42. Engelhardt S, Lee J, Gäbler Y, Kemmerling B, Haapalainen M-L. 42.  et al. 2009. Separable roles of the Pseudomonas syringae pv. phaseolicola accessory protein HrpZ1 in ion-conducting pore formation and activation of plant immunity. Plant J. 57:706–17 [Google Scholar]
  43. Fargier E, Fischer-Le Saux M, Manceau C. 43.  2011. A multilocus sequence analysis of Xanthomonas campestris reveals a complex structure within crucifer-attacking pathovars of this species. Syst. Appl. Microbiol. 34:156–65 [Google Scholar]
  44. Feil EJ, Holmes EC, Bessen DE, Chan M-S, Day NPJ. 44.  et al. 2001. Recombination within natural populations of pathogenic bacteria: Short-term empirical estimates and long-term phylogenetic consequences. Proc. Natl. Acad. Sci. USA 98:182–87 [Google Scholar]
  45. Felix G, Boller T. 45.  2003. Molecular sensing of bacteria in plants: the highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278:6201–8 [Google Scholar]
  46. Felix G, Duran JD, Volko S, Boller T. 46.  1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18:265–76 [Google Scholar]
  47. Feng F, Zhou J-M. 47.  2012. Plant–bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15:469–76 [Google Scholar]
  48. Feng J, Schuenzel EL, Li J, Schaad NW. 48.  2009. Multilocus sequence typing reveals two evolutionary lineages of Acidovorax avenae subsp. citrulli. Phytopathology 99:913–20 [Google Scholar]
  49. Ferrante P, Clarke CR, Cavanaugh KA, Michelmore RW, Buonaurio R, Vinatzer BA. 49.  2009. Contributions of the effector gene hopQ1-1 to differences in host range between Pseudomonas syringae pv. phaseolicola and P. syringae pv. tabaci. Mol. Plant Pathol. 10:837–42 [Google Scholar]
  50. Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GCM, Joosten MHAJ, Thomma BPHJ. 50.  2011. Interfamily transfer of tomato ve1 mediates verticillium resistance in Arabidopsis. Plant Physiol. 156:2255–65 [Google Scholar]
  51. Fraser C, Hanage WP, Spratt BG. 51.  2007. Recombination and the nature of bacterial speciation. Science 315:476–80 [Google Scholar]
  52. Gardan L, Shafik H, Belouin S, Broch R, Grimont F, Grimont PAD. 52.  1999. 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. 49:469–78 [Google Scholar]
  53. Gassmann W, Dahlbeck D, Chesnokova O, Minsavage GV, Jones JB, Staskawicz BJ. 53.  2000. Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 182:7053–59 [Google Scholar]
  54. Genin S, Denny TP. 54.  2012. Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50:67–89 [Google Scholar]
  55. Gerlach G, von Wintzingerode F, Middendorf B, Gross R. 55.  2001. Evolutionary trends in the genus Bordetella. Microbes Infect. 3:61–72 [Google Scholar]
  56. Glasner JD, Marquez-Villavicencio M, Kim HS, Jahn CE, Ma B. 56.  et al. 2008. Niche-specificity and the variable fraction of the pectobacterium pan-genome. Mol. Plant-Microbe Interact. 21:1549–60 [Google Scholar]
  57. Goss EM, Kreitman M, Bergelson J. 57.  2005. Genetic diversity, recombination and cryptic clades in Pseudomonas viridiflava infecting natural populations of Arabidopsis thaliana. Genetics 169:21–35 [Google Scholar]
  58. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL. 58.  2006. Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60:425–49 [Google Scholar]
  59. Green S, Studholme DJ, Laue BE, Dorati F, Lovell H. 59.  et al. 2010. Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS ONE 5:e10224 [Google Scholar]
  60. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. 60.  2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722–26 [Google Scholar]
  61. Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C. 61.  et al. 2009. A “repertoire for repertoire” hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas. PLoS ONE 4:e6632 [Google Scholar]
  62. Hamza AA, Robene-Soustrade I, Jouen E, Lefeuvre P, Chiroleu F. 62.  et al. 2012. Multilocus sequence analysis– and amplified fragment length polymorphism–based characterization of xanthomonads associated with bacterial spot of tomato and pepper and their relatedness to Xanthomonas species. Syst. Appl. Microbiol. 35:183–90 [Google Scholar]
  63. Hanage WP, Fraser C, Spratt BG. 63.  2006. Sequences, sequence clusters and bacterial species. Philos. Trans. R. Soc. B 361:1917–27 [Google Scholar]
  64. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill F-X. 64.  et al. 2008. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat. Genet. 40:987–93 [Google Scholar]
  65. Hwang MS, Morgan RL, Sarkar SF, Wang PW, Guttman DS. 65.  2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 71:5182–91 [Google Scholar]
  66. Islam M-S, Glynn J, Bai Y, Duan Y-P, Coletta-Filho H. 66.  et al. 2012. Multilocus microsatellite analysis of “Candidatus Liberibacter asiaticus” associated with citrus Huanglongbing worldwide. BMC Microbiol. 12:39 [Google Scholar]
  67. Jackson RW, Vinatzer B, Arnold DL, Dorus S, Murillo J. 67.  2011. The influence of the accessory genome on bacterial pathogen evolution. Mobile Genet. Elem. 1:55–65 [Google Scholar]
  68. Jacques MA, Durand K, Orgeur G, Balidas S, Fricot C. 68.  et al. 2012. Phylogenetic analysis and polyphasic characterization of Clavibacter michiganensis strains isolated from tomato seeds reveal that nonpathogenic strains are distinct from C. michiganensis subsp. michiganensis. Appl. Environ. Microbiol. 78:8388–402 [Google Scholar]
  69. Jones JDG, Dangl JL. 69.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  70. Katagiri F, Tsuda K. 70.  2010. Understanding the plant immune system. Mol. Plant-Microbe Interact. 23:1531–36 [Google Scholar]
  71. Kim HS, Ma B, Perna NT, Charkowski AO. 71.  2009. Phylogeny and virulence of naturally occurring type III secretion system-deficient Pectobacterium strains. Appl. Environ. Microbiol. 75:4539–49 [Google Scholar]
  72. Kung SH, Almeida RP. 72.  2011. Natural competence and recombination in the plant pathogen Xylella fastidiosa. Appl. Environ. Microbiol. 77:5278–84 [Google Scholar]
  73. Kunkeaw S, Tan S, Coaker G. 73.  2010. Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol. Plant-Microbe Interact. 23:415–24 [Google Scholar]
  74. Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. 74.  2004. The N terminus of bacterial elongation factor tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–507 [Google Scholar]
  75. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D. 75.  et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365–69 [Google Scholar]
  76. Lin N-C, Martin GB. 76.  2005. An avrPto/avrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol. Plant-Microbe Interact. 18:43–51 [Google Scholar]
  77. Lloyd SR, Schoonbeek H-j, Trick M, Zipfel C, Ridout CJ. 77.  2013. Methods to study PAMP-triggered immunity in Brassica species. Mol. Plant-Microbe Interact. 27:286–95 [Google Scholar]
  78. Lovell HC, Mansfield JW, Godfrey SAC, Jackson RW, Hancock JT, Arnold DL. 78.  2009. Bacterial evolution by genomic island transfer occurs via DNA transformation in planta. Curr. Biol. 19:1586–90 [Google Scholar]
  79. Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE. 79.  et al. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95:3140–45 [Google Scholar]
  80. Malnoy M, Martens S, Norelli JL, Barny MA, Sundin GW. 80.  et al. 2012. Fire blight: applied genomic insights of the pathogen and host. Annu. Rev. Phytopathol. 50:475–94 [Google Scholar]
  81. Mann RA, Smits THM, Buhlmann A, Blom J, Goesmann A. 81.  et al. 2013. Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS ONE 8:e55644 [Google Scholar]
  82. Mazzaglia A, Studholme DJ, Taratufolo MC, Cai R, Almeida NF. 82.  et al. 2012. Pseudomonas syringae pv. actinidiae (PSA) isolates from recent bacterial canker of kiwifruit outbreaks belong to the same genetic lineage. PLoS ONE 7:e57464 [Google Scholar]
  83. McAdam PR, Templeton KE, Edwards GF, Holden MTG, Feil EJ. 83.  et al. 2012. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 109:9107–12 [Google Scholar]
  84. McCann HC, Nahal H, Thakur S, Guttman DS. 84.  2012. Identification of innate immunity elicitors using molecular signatures of natural selection. Proc. Natl. Acad. Sci. USA 109:4215–20 [Google Scholar]
  85. McCann HC, Rikkerink EHA, Bertels F, Fiers M, Lu A. 85.  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 [Google Scholar]
  86. Mhedbi-Hajri N, Darrasse A, Pigne S, Durand K, Fouteau S. 86.  et al. 2011. Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads. BMC Evol. Biol. 11:67 [Google Scholar]
  87. Mhedbi-Hajri N, Hajri A, Boureau T, Darrasse A, Durand K. 87.  et al. 2013. Evolutionary history of the plant pathogenic bacterium Xanthomonas axonopodis. PLoS ONE 8:e58474 [Google Scholar]
  88. Michelmore RW, Christopoulou M, Caldwell KS. 88.  2013. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu. Rev. Phytopathol. 51:291–319 [Google Scholar]
  89. Milijašević-Marčić S, Gartemann K-H, Frohwitter J, Eichenlaub R, Todorović B. 89.  et al. 2012. Characterization of Clavibacter michiganensis subsp. michiganensis strains from recent outbreaks of bacterial wilt and canker in Serbia. Eur. J. Plant Pathol. 134:697–711 [Google Scholar]
  90. Mohr TJ, Liu H, Yan S, Morris CE, Castillo JA. 90.  et al. 2008. Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues. J. Bacteriol. 190:2858–70 [Google Scholar]
  91. Monaghan J, Zipfel C. 91.  2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349–57 [Google Scholar]
  92. Monteil CL, Cai R, Liu H, Mechan Llontop ME, Leman S. 92.  et al. 2013. Non-agricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens. New Phytol. 199:800–11 [Google Scholar]
  93. Monteil CL, Guilbaud C, Glaux C, Lafolie F, Soubeyrand S, Morris CE. 93.  2012. Emigration of the plant pathogen Pseudomonas syringae from leaf litter contributes to its population dynamics in alpine snowpack. Environ. Microbiol. 14:2099–112 [Google Scholar]
  94. Morelli G, Didelot X, Kusecek B, Schwarz S, Bahlawane C. 94.  et al. 2010. Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet. 6:e1001036 [Google Scholar]
  95. Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P. 95.  et al. 2010. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 42:1140–43 [Google Scholar]
  96. Morris CE, Monteil CL, Berge O. 96.  2013. The life history of Pseudomonas syringae: linking agriculture and Earth system processes. Annu. Rev. Phytopathol. 51:85–104 [Google Scholar]
  97. Morris CE, Sands DC, Vanneste JL, Montarry J, Oakley B. 97.  et al. 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 1:1–10 [Google Scholar]
  98. Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C. 98.  et al. 2008. The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J. 2:321–34 [Google Scholar]
  99. Mueller K, Chinchilla D, Albert M, Jehle AK, Kalbacher H. 99.  et al. 2012. Contamination risks in work with synthetic peptides: flg22 as an example of a pirate in commercial peptide preparations. Plant Cell 24:3193–97 [Google Scholar]
  100. Nosil P, Funk DJ, Ortiz-Barrientos D. 100.  2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18:375–402 [Google Scholar]
  101. Nübel U, Dordel J, Kurt K, Strommenger B, Westh H. 101.  et al. 2010. A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog. 6:e100855 [Google Scholar]
  102. Nübel U, Roumagnac P, Feldkamp M, Song J-H, Ko KS. 102.  et al. 2008. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 105:14130–35 [Google Scholar]
  103. Nunney L, Yuan X, Bromley R, Hartung J, Montero-Astua M. 103.  et al. 2010. 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 5:e15488 [Google Scholar]
  104. Nunney L, Yuan X, Bromley RE, Stouthamer R. 104.  2012. Detecting genetic introgression: high levels of intersubspecific recombination found in Xylella fastidiosa in Brazil. Appl. Environ. Microbiol. 78:4702–14 [Google Scholar]
  105. Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M. 105.  et al. 2012. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog. 8:e1003013 [Google Scholar]
  106. O'Brien H, Thakur S, Gong Y, Fung P, Zhang J. 106.  et al. 2012. Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol. 12:141 [Google Scholar]
  107. Patil P, Bogdanove A, Sonti R. 107.  2007. The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice, citrus and crucifers. BMC Evol. Biol. 7:243 [Google Scholar]
  108. Pitman AR, Jackson RW, Mansfield JW, Kaitell V, Thwaites R, Arnold DL. 108.  2005. Exposure to host resistance mechanisms drives evolution of bacterial virulence in plants. Curr. Biol. 15:2230–35 [Google Scholar]
  109. Potnis N, Krasileva K, Chow V, Almeida NF, Patil PB. 109.  et al. 2011. Comparative genomics reveals diversity among xanthomonads infecting tomato and pepper. BMC Genomics 12:146 [Google Scholar]
  110. Prior P, Fegan M. 110.  2005. Recent development in the phylogeny and classification of Ralstonia solanacearum. Proceedings of the First International Symposium on Tomato Diseases T Momol, JB Jones 127–36 Leuven, Belgium: ISHS-Acta Horticulturae
  111. Purcell AH, Hopkins DL. 111.  1996. Fastidious xylem-limited bacterial plant pathogens. Annu. Rev. Phytopathol. 34:131–51 [Google Scholar]
  112. Remenant B, Coupat-Goutaland B, Guidot A, Cellier G, Wicker E. 112.  et al. 2010. Genomes of three tomato pathogens within the Ralstonia solanacearum species complex reveal significant evolutionary divergence. BMC Genomics 11:379 [Google Scholar]
  113. Remenant B, de Cambiaire J-C, Cellier G, Jacobs JM, Mangenot S. 113.  et al. 2011. Ralstonia syzygii, the blood disease bacterium and some asian R. solanacearum strains form a single genomic species despite divergent lifestyles. PLoS ONE 6:e24356 [Google Scholar]
  114. Sabbagh SC, Forest CG, Lepage C, Leclerc J-M, Daigle F. 114.  2010. So similar, yet so different: uncovering distinctive features in the genomes of Salmonella enterica serovars Typhimurium and Typhi. FEMS Microbiol. Lett. 305:1–13 [Google Scholar]
  115. Sarkar SF, Gordon JS, Martin GB, Guttman DS. 115.  2006. Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 174:1041–56 [Google Scholar]
  116. Sarkar SF, Guttman DS. 116.  2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl. Environ. Microbiol. 70:1999–2012 [Google Scholar]
  117. Scally M, Schuenzel EL, Stouthamer R, Nunney L. 117.  2005. Multilocus sequence type system for the plant pathogen Xylella fastidiosa and relative contributions of recombination and point mutation to clonal diversity. Appl. Environ. Microbiol. 71:8491–99 [Google Scholar]
  118. Schuenzel EL, Scally M, Stouthamer R, Nunney L. 118.  2005. A multigene phylogenetic study of clonal diversity and divergence in North American strains of the plant pathogen Xylella fastidiosa. Appl. Environ. Microbiol. 71:3832–39 [Google Scholar]
  119. Shapiro BJ, Friedman J, Cordero OX, Preheim SP, Timberlake SC. 119.  et al. 2012. Population genomics of early events in the ecological differentiation of bacteria. Science 336:48–51 [Google Scholar]
  120. Shendure J, Ji H. 120.  2008. Next-generation DNA sequencing. Nat. Biotechnol. 26:1135–45 [Google Scholar]
  121. Sheppard SK, Didelot X, Meric G, Torralbo A, Jolley KA. 121.  et al. 2013. Genome-wide association study identifies vitamin B-5 biosynthesis as a host specificity factor in Campylobacter. Proc. Natl. Acad. Sci. USA 110:11923–27 [Google Scholar]
  122. Smith JM, Smith NH, O'Rourke M, Spratt BG. 122.  1993. How clonal are bacteria?. Proc. Natl. Acad. Sci. USA 90:4384–88 [Google Scholar]
  123. Smith KD, Andersen-Nissen E, Hayashi F, Strobe K, Bergman MA. 123.  et al. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4:1247–53 [Google Scholar]
  124. Smits THM, Rezzonico F, Duffy B. 124.  2011. Evolutionary insights from Erwinia amylovora genomics. J. Biotechnol. 155:34–39 [Google Scholar]
  125. Smits THM, Rezzonico F, Kamber T, Blom J, Goesmann A. 125.  et al. 2010. Complete genome sequence of the fire blight pathogen Erwinia amylovora CFBP 1430 and comparison to other Erwinia spp. Mol. Plant-Microbe Interact. 23:384–93 [Google Scholar]
  126. Stukenbrock EH, McDonald BA. 126.  2008. The origins of plant pathogens in agro-ecosystems. Annu. Rev. Phytopathol. 46:75–100 [Google Scholar]
  127. Sun W, Dunning FM, Pfund C, Weingarten R, Bent AF. 127.  2006. Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2–dependent defenses. Plant Cell 18:764–79 [Google Scholar]
  128. Tanaka N, Che F-S, Watanabe N, Fujiwara S, Takayama S, Isogai A. 128.  2003. Flagellin from an incompatible strain of Acidovorax avenae mediates H2O2 generation accompanying hypersensitive cell death and expression of PAL, Cht-1, and PBZ1, but not of LOX in rice. Mol. Plant-Microbe Interact. 16:422–28 [Google Scholar]
  129. Tsunemi K, Taguchi F, Marutani M, Watanabe-Sugimoto M, Inagaki Y. 129.  et al. 2011. Degeneration of hrpZ gene in Pseudomonas syringae pv. tabaci to evade tobacco defence: an arms race between tobacco and its bacterial pathogen. Mol. Plant Pathol. 12:709–14 [Google Scholar]
  130. Vetter MM, Kronholm I, He F, Häweker H, Reymond M. 130.  et al. 2012. Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29:1655–67 [Google Scholar]
  131. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R. 131.  et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49:507–31 [Google Scholar]
  132. Wang PW, Morgan RL, Scortichini M, Guttman DS. 132.  2007. Convergent evolution of phytopathogenic pseudomonads onto hazelnut. Microbiology 153:2067–73 [Google Scholar]
  133. Wasukira A, Tayebwa J, Thwaites R, Paszkiewicz K, Aritua V. 133.  et al. 2012. Genome-wide sequencing reveals two major sub-lineages in the genetically monomorphic pathogen Xanthomonas campestris pv. musacearum. Genes 3:361–77 [Google Scholar]
  134. Wicker E, Lefeuvre P, de Cambiaire JC, Lemaire C, Poussier S, Prior P. 134.  2012. Contrasting recombination patterns and demographic histories of the plant pathogen Ralstonia solanacearum inferred from MLSA. ISME J. 6:961–74 [Google Scholar]
  135. Willis DK, Kinscherf TG. 135.  2009. Population dynamics of Pseudomonas syringae pv. tomato strains on tomato cultivars Rio Grande and Rio Grande-Pto under field conditions. J. Phytopathol. 157:219–27 [Google Scholar]
  136. Yan S, Liu H, Mohr TJ, Jenrette J, Chiodini R. 136.  et al. 2008. Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Appl. Environ. Microbiol. 74:3171–81 [Google Scholar]
  137. Young BC, Golubchik T, Batty EM, Fung R, Larner-Svensson H. 137.  et al. 2012. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc. Natl. Acad. Sci. USA 109:4550–55 [Google Scholar]
  138. Young JM, Park DC, Shearman HM, Fargier E. 138.  2008. A multilocus sequence analysis of the genus Xanthomonas. Syst. Appl. Microbiol. 31:366–77 [Google Scholar]
  139. Yuan X, Morano L, Bromley R, Spring-Pearson S, Stouthamer R, Nunney L. 139.  2010. Multilocus sequence typing of Xylella fastidiosa causing Pierce's disease and oleander leaf scorch in the United States. Phytopathology 100601–11 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
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