1932

Abstract

Trade in plant and plant products has profoundly affected the global distribution and diversity of plant pathogens. Identification of migration pathways can be used to monitor or manage pathogen movement for proactive disease management or quarantine measures. Genomics-based genetic marker discovery is allowing unprecedented collection of population genetic data for plant pathogens. These data can be used for detailed analysis of the ancestry of population samples and therefore for analysis of migration. Reconstruction of migration histories has confirmed previous hypotheses based on observational data and led to unexpected new findings on the origins of pathogens and source populations for past and recent migration. The choice of software for analysis depends on the type of migration being studied and the reproductive mode of the pathogen. Biased sampling and complex population structures are potential challenges to accurate inference of migration pathways.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080614-115936
2015-08-04
2024-04-14
Loading full text...

Full text loading...

/deliver/fulltext/phyto/53/1/annurev-phyto-080614-115936.html?itemId=/content/journals/10.1146/annurev-phyto-080614-115936&mimeType=html&fmt=ahah

Literature Cited

  1. Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF. 1.  et al. 2014. Origin, migration routes and worldwide population genetic structure of the wheat yellow rust Puccinia striiformis f. sp. tritici. PLOS Pathog. 10:e1003903 [Google Scholar]
  2. Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P. 2.  2004. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19:535–44 [Google Scholar]
  3. Atallah ZK, Maruthachalam K, du Toit L, Koike ST, Davis RM. 3.  et al. 2010. Population analyses of the vascular plant pathogen Verticillium dahliae detect recombination and transcontinental gene flow. Fungal Genet. Biol. 47:416–22 [Google Scholar]
  4. Banke S, McDonald BA. 4.  2005. Migration patterns among global populations of the pathogenic fungus Mycosphaerella graminicola. Mol. Ecol. 14:1881–96 [Google Scholar]
  5. Barres B, Carlier J, Seguin M, Fenouillet C, Cilas C, Ravigne V. 5.  2012. Understanding the recent colonization history of a plant pathogenic fungus using population genetic tools and approximate Bayesian computation. Heredity 109:269–79 [Google Scholar]
  6. Bebber DP, Holmes T, Gurr SJ. 6.  2014. The global spread of crop pests and pathogens. Glob. Ecol. Biogeogr. 23:1398–407 [Google Scholar]
  7. Beerli P. 7.  2007. Estimation of the population scaled mutation rate from microsatellite data. Genetics 177:1967–68 [Google Scholar]
  8. Beerli P. 8.  2009. How to use Migrate or why are Markov chain Monte Carlo programs difficult to use?. Population Genetics for Animal Conservation G Bertorelle, MW Bruford, HC Hauffe, A Rizzoli, C Vernesi 42–79 Cambridge: Cambridge Univ. Press [Google Scholar]
  9. Beerli P, Felsenstein J. 9.  2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc. Natl. Acad. Sci. USA 98:4563–68 [Google Scholar]
  10. Beerli P, Palczewski M. 10.  2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–26 [Google Scholar]
  11. Bernardes-de-Assis J, Storari M, Zala M, Wang W, Jiang D. 11.  et al. 2009. Genetic structure of populations of the rice-infecting pathogen Rhizoctonia solani AG-1 IA from China. Phytopathology 99:1090–99 [Google Scholar]
  12. Bertorelle G, Benazzo A, Mona S. 12.  2010. ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol. Ecol. 19:2609–25 [Google Scholar]
  13. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H. 13.  et al. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Comput. Biol. 10:e1003537 [Google Scholar]
  14. Brasier CM. 14.  2008. The biosecurity threat to the UK and global environment from international trade in plants. Plant Pathol. 57:792–808 [Google Scholar]
  15. Brown JKM, Hovmoller MS. 15.  2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–41 [Google Scholar]
  16. Brunner PC, Schuerch S, McDonald BA. 16.  2007. The origin and colonization history of the barley scald pathogen Rhynchosporium secalis. J. Evol. Biol. 20:1311–21 [Google Scholar]
  17. Bryner SF, Rigling D, Brunner PC. 17.  2012. Invasion history and demographic pattern of Cryphonectria hypovirus 1 across European populations of the chestnut blight fungus. Ecol. Evol. 2:3227–41 [Google Scholar]
  18. Cai R, Lewis J, Yan S, Liu H, Clarke CR. 18.  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]
  19. Ceresini PC, Shew HD, James TY, Vilgalys RJ, Cubeta MA. 19.  2007. Phylogeography of the Solanaceae-infecting Basidiomycota fungus Rhizoctonia solani AG-3 based on sequence analysis of two nuclear DNA loci. BMC Evol. Biol. 7:163 [Google Scholar]
  20. Corander J, Marttinen P, Siren J, Tang J. 20.  2008. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform. 9:539 [Google Scholar]
  21. Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M. 21.  et al. 2014. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–89 [Google Scholar]
  22. Croucher PJP, Mascheretti S, Garbelotto M. 22.  2013. Combining field epidemiological information and genetic data to comprehensively reconstruct the invasion history and the microevolution of the sudden oak death agent Phytophthora ramorum (Stramenopila: Oomycetes) in California. Biol. Invasions 15:2281–97 [Google Scholar]
  23. Csilléry K, Blum MGB, Gaggiotti OE, Francois O. 23.  2010. Approximate Bayesian computation (ABC) in practice. Trends Ecol. Evol. 25:410–18 [Google Scholar]
  24. Csilléry K, François O, Blum MGB. 24.  2012. abc: an R package for approximate Bayesian computation (ABC). Methods Ecol. Evol. 3:475–79 [Google Scholar]
  25. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. 25.  2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12:499–510 [Google Scholar]
  26. De Bruyn A, Villemot J, Lefeuvre P, Villar E, Hoareau M. 26.  et al. 2012. East African cassava mosaic-like viruses from Africa to Indian ocean islands: molecular diversity, evolutionary history and geographical dissemination of a bipartite begomovirus. BMC Evol. Biol. 12:228 [Google Scholar]
  27. Drummond AJ, Suchard MA, Xie D, Rambaut A. 27.  2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969–73 [Google Scholar]
  28. Dutech C, Barres B, Bridier J, Robin C, Milgroom M, Ravigne V. 28.  2012. The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen. Mol. Ecol. 21:3931–46 [Google Scholar]
  29. Ellegren H. 29.  2004. Microsatellites: simple sequences with complex evolution. Nat. Rev. Genet. 5:435–45 [Google Scholar]
  30. Estoup A, Guillemaud T. 30.  2010. Reconstructing routes of invasion using genetic data: why, how and so what?. Mol. Ecol. 19:4113–30 [Google Scholar]
  31. Gau RD, Merz U, Falloon RE, Brunner PC. 31.  2013. Global genetics and invasion history of the potato powdery scab pathogen, Spongospora subterranea f. sp. subterranea. PLOS ONE 8:e67944 [Google Scholar]
  32. Gladieux P, Feurtey A, Hood ME, Snirc A, Clavel J. 32.  et al. 2015. The population biology of fungal invasions. Mol. Ecol. 241969–86
  33. Gladieux P, Zhang X-G, Afoufa-Bastien D, Sanhueza R-MV, Sbaghi M, Le Cam B. 33.  2008. On the origin and spread of the scab disease of apple: out of central Asia. PLOS ONE 3:e1455 [Google Scholar]
  34. Goss EM, Larsen M, Vercauteren A, Werres S, Heungens K, Grünwald NJ. 34.  2011. Phytophthora ramorum in Canada: evidence for migration within North America and from Europe. Phytopathology 101:166–71 [Google Scholar]
  35. Goss EM, Larsen MM, Chastagner GA, Givens DR, Grünwald NJ. 35.  2009. Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLOS Pathog. 5:e1000583 [Google Scholar]
  36. Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE. 36.  et al. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proc. Natl. Acad. Sci. USA 111:8791–96 [Google Scholar]
  37. Grünwald NJ, Flier WG. 37.  2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171–90 [Google Scholar]
  38. Grünwald NJ, Goss EM. 38.  2011. Evolution and population genetics of exotic and re-emerging pathogens: novel tools and approaches. Annu. Rev. Phytopathol. 49:249–67 [Google Scholar]
  39. Guillot G, Santos F, Estoup A. 39.  2008. Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–7 [Google Scholar]
  40. Gurung S, Short DPG, Adhikari TB. 40.  2013. Global population structure and migration patterns suggest significant population differentiation among isolates of Pyrenophora tritici-repentis. Fungal Genet. Biol. 52:32–41 [Google Scholar]
  41. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 41.  2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5:e1000695 [Google Scholar]
  42. Hey J. 42.  2010. The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol. Biol. Evol. 27:921–33 [Google Scholar]
  43. Hey J. 43.  2010. Isolation with migration models for more than two populations. Mol. Biol. Evol. 27:905–20 [Google Scholar]
  44. Holsinger KE, Weir BS. 44.  2009. Genetics in geographically structured populations: defining, estimating and interpreting FST. Nat. Rev. Genet. 10:639–50 [Google Scholar]
  45. Jombart T, Devillard S, Balloux F. 45.  2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11:94 [Google Scholar]
  46. Kuhner MK. 46.  2006. LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–70 [Google Scholar]
  47. Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJA. 47.  et al. 2010. The spread of Tomato yellow leaf curl virus from the Middle East to the world. PLOS Pathog. 6:e1001164 [Google Scholar]
  48. Lemey P, Rambaut A, Drummond AJ, Suchard MA. 48.  2009. Bayesian phylogeography finds its roots. PLOS Comput. Biol. 5:e1000520 [Google Scholar]
  49. Lemey P, Rambaut A, Welch JJ, Suchard MA. 49.  2010. Phylogeography takes a relaxed random walk in continuous space and time. Mol. Biol. Evol. 27:1877–85 [Google Scholar]
  50. Linde CC, Zala M, McDonald BA. 50.  2009. Molecular evidence for recent founder populations and human-mediated migration in the barley scald pathogen Rhynchosporium secalis. Mol. Phylogenet. Evol. 51:454–64 [Google Scholar]
  51. Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A. 51.  2010. Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLOS ONE 5:e9743 [Google Scholar]
  52. Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B. 52.  et al. 2014. Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol. Ecol 23:5979–97 [Google Scholar]
  53. Martin MD, Ho SYW, Wales N, Ristaino JB, Gilbert MTP. 53.  2014. Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant New World Phytophthora infestans. Mol. Biol. Evol. 31:1414–20 [Google Scholar]
  54. Mascheretti S, Croucher PJP, Kozanitas M, Baker L, Garbelotto M. 54.  2009. Genetic epidemiology of the Sudden Oak Death pathogen Phytophthora ramorum in California. Mol. Ecol. 18:4577–90 [Google Scholar]
  55. Mascheretti S, Croucher PJP, Vettraino A, Prospero S, Garbelotto M. 55.  2008. Reconstruction of the Sudden Oak Death epidemic in California through microsatellite analysis of the pathogen Phytophthora ramorum. Mol. Ecol. 17:2755–68 [Google Scholar]
  56. McDonald BA, Linde C. 56.  2002. Pathogen population genetics, evolutionary potential, and durable resistance. Annu. Rev. Phytopathol. 40:349–79 [Google Scholar]
  57. Monjane AL, Harkins GW, Martin DP, Lemey P, Lefeuvre P. 57.  et al. 2011. Reconstructing the history of maize streak virus strain A dispersal to reveal diversification hot spots and its origin in southern Africa. J. Virol. 85:9623–36 [Google Scholar]
  58. Morin L, Gomez DR, Evans KJ, Neill TM, Mahaffee WF, Linde CC. 58.  2013. Invaded range of the blackberry pathogen Phragmidium violaceum in the Pacific Northwest of the USA and the search for its provenance. Biol. Invasions 15:1847–61 [Google Scholar]
  59. Mundt C, Wallace L, Allen T, Hollier C, Kemerait R, Sikora E. 59.  2013. Initial epidemic area is strongly associated with the yearly extent of soybean rust spread in North America. Biol. Invasions 15:1431–38 [Google Scholar]
  60. Munkacsi AB, Stoxen S, May G. 60.  2008. Ustilago maydis populations tracked maize through domestication and cultivation in the Americas. Proc. R. Soc. B 275:1037–46 [Google Scholar]
  61. Nielsen R, Paul JS, Albrechtsen A, Song YS. 61.  2011. Genotype and SNP calling from next-generation sequencing data. Nat. Rev. Genet. 12:443–451 [Google Scholar]
  62. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A. 62.  2004. GENECLASS2: A software for genetic assignment and first-generation migrant detection. J. Heredity 95:536–39 [Google Scholar]
  63. Pritchard JK, Stephens M, Donnelly P. 63.  2000. Inference of population structure from multilocus genotype data. Genetics 155:945–59 [Google Scholar]
  64. Prospero S, Grünwald NJ, Winton LM, Hansen EM. 64.  2009. Migration patterns of the emerging plant pathogen Phytophthora ramorum on the West Coast of the United States of America. Phytopathology 99:739–49 [Google Scholar]
  65. Quesada-Ocampo L, Granke L, Olsen J, Gutting HC, Runge F. 65.  et al. 2012. The genetic structure of Pseudoperonospora cubensis populations. Plant Dis 96:1459–70 [Google Scholar]
  66. Saleh D, Xu P, Shen Y, Li C, Adreit H. 66.  et al. 2012. Sex at the origin: an Asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol. Ecol. 21:1330–44 [Google Scholar]
  67. Schoebel CN, Stewart J, Gruenwald NJ, Rigling D, Prospero S. 67.  2014. Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLOS ONE 9:e105259 [Google Scholar]
  68. Sjoholm L, Andersson B, Hogberg N, Widmark A-K, Yuen J. 68.  2013. Genotypic diversity and migration patterns of Phytophthora infestans in the Nordic countries. Fungal Biol. 117:722–30 [Google Scholar]
  69. Sousa W, Hey J. 69.  2013. Understanding the origin of species with genome-scale data: modelling gene flow. Nat. Rev. Genet. 14:404–14 [Google Scholar]
  70. Stukenbrock EH, Banke S, McDonald BA. 70.  2006. Global migration patterns in the fungal wheat pathogen Phaeosphaeria nodorum. Mol. Ecol. 15:2895–904 [Google Scholar]
  71. Timilsina S, Jibrin MO, Potnis N, Minsavage GV, Kebede M. 71.  et al. 2015. Multilocus sequence analysis of xanthomonads causing bacterial spot of tomato and pepper reveals strains generated by recombination among species and recent global spread of Xanthomonas gardneri. Appl. Environ. Microbiol. In press. doi:10.1128/AEM.03000-14
  72. Tsui CKM, Roe AD, El-Kassaby YA, Rice AV, Alamouti SM. 72.  et al. 2012. Population structure and migration pattern of a conifer pathogen, Grosmannia clavigera, as influenced by its symbiont, the mountain pine beetle. Mol. Ecol. 21:71–86 [Google Scholar]
  73. Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L. 73.  2010. ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinform. 11:116 [Google Scholar]
  74. Wei N, Bemmels JB, Dick CW. 74.  2014. The effects of read length, quality and quantity on microsatellite discovery and primer development: from Illumina to PacBio. Mol. Ecol. Resour. 14:953–65 [Google Scholar]
  75. Wichmann G, Ritchie D, Kousik C, Bergelson J. 75.  2005. Reduced genetic variation occurs among genes of the highly clonal plant pathogen Xanthomonas axonopodis pv. vesicatoria, including the effector gene avrBs2. Appl. Environ. Microbiol. 71:2418–32 [Google Scholar]
  76. Wilson GA, Rannala B. 76.  2003. Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–91 [Google Scholar]
  77. Xhaard C, Barres B, Andrieux A, Bousset L, Halkett F, Frey P. 77.  2012. Disentangling the genetic origins of a plant pathogen during disease spread using an original molecular epidemiology approach. Mol. Ecol. 21:2383–98 [Google Scholar]
  78. Yasaka R, Nguyen HD, Ho SYW, Duchene S, Korkmaz S. 78.  et al. 2014. The temporal evolution and global spread of Cauliflower mosaic virus, a plant pararetrovirus. PLOS ONE 9:e95410 [Google Scholar]
  79. Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B. 79.  et al. 2013. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. eLife 2:e00731 [Google Scholar]
  80. Zaffarano PL, McDonald BA, Linde CC. 80.  2009. Phylogeographical analyses reveal global migration patterns of the barley scald pathogen Rhynchosporium secalis. Mol. Ecol. 18:279–93 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080614-115936
Loading
/content/journals/10.1146/annurev-phyto-080614-115936
Loading

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