1932

Abstract

We are entering a new era in plant pathology in which whole-genome sequences of many individuals of a pathogen species are becoming readily available. Population genomics aims to discover genetic mechanisms underlying phenotypes associated with adaptive traits such as pathogenicity, virulence, fungicide resistance, and host specialization, as genome sequences or large numbers of single nucleotide polymorphisms become readily available from multiple individuals of the same species. This emerging field encompasses detailed genetic analyses of natural populations, comparative genomic analyses of closely related species, identification of genes under selection, and linkage analyses involving association studies in natural populations or segregating populations resulting from crosses. The era of pathogen population genomics will provide new opportunities and challenges, requiring new computational and analytical tools. This review focuses on conceptual and methodological issues as well as the approaches to answering questions in population genomics. The major steps start with defining relevant biological and evolutionary questions, followed by sampling, genotyping, and phenotyping, and ending in analytical methods and interpretations. We provide examples of recent applications of population genomics to fungal and oomycete plant pathogens.

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2016-08-04
2024-06-19
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Literature Cited

  1. Aguileta G, Refrégier G, Yockteng R, Fournier E, Giraud T. 1.  2009. Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect. Genet. Evol. 9:4656–70 [Google Scholar]
  2. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. 2.  2016. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat. Rev. Genet. 17:281–92Discusses the challenges of SNP genotyping and analysis from reduced-representation sequencing. [Google Scholar]
  3. Andrews KR, Luikart G. 3.  2014. Recent novel approaches for population genomics data analysis. Mol. Ecol. 23:71661–67 [Google Scholar]
  4. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL. 4.  et al. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLOS ONE 3:10e3376 [Google Scholar]
  5. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. 5.  2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:192633–35 [Google Scholar]
  6. Browning BL, Browning SR. 6.  2016. Genotype imputation with millions of reference samples. Am. J. Hum. Genet. 98:1116–26 [Google Scholar]
  7. Browning SR. 7.  2008. Missing data imputation and haplotype phase inference for genome-wide association studies. Hum. Genet. 124:5439–50 [Google Scholar]
  8. Browning SR, Browning BL. 8.  2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81:51084–97 [Google Scholar]
  9. Browning SR, Browning BL. 9.  2011. Haplotype phasing: existing methods and new developments. Nat. Rev. Genet. 12:10703–14 [Google Scholar]
  10. Brunner PC, Stefanato FL, McDonald BA. 10.  2008. Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol. Plant Pathol. 9:3305–16 [Google Scholar]
  11. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA. 11.  2013. Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol. Biol. Evol. 30:61337–47 [Google Scholar]
  12. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA. 12.  2014. Hitchhiking selection is driving intron gain in a pathogenic fungus. Mol. Biol. Evol. 31:71741–49 [Google Scholar]
  13. Callaway E. 13.  2016. Devastating wheat fungus appears in Asia for first time. Nature 532:421–22 [Google Scholar]
  14. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 14.  2009. The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233–38 [Google Scholar]
  15. Castroagudín VL, Ceresini PC, de Oliveira SC, Reges JTA, Maciel JLN. 15.  et al. 2015. Resistance to QoI fungicides is widespread in Brazilian populations of the wheat blast pathogen Magnaporthe oryzae. Phytopathology 105:3284–94 [Google Scholar]
  16. Castroagudín VL, Moreira SI, Pereira DAS, Moreira SS, Brunner PC. 16.  et al. 2016. Pyricularia graminis-tritici sp. nov., a new Pyricularia species causing wheat blast.. Persoonia. In press [Google Scholar]
  17. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH, De Koning D-J. 17.  2011. Stacks: building and genotyping loci de novo from short-read sequences. G3 1:3171–82 [Google Scholar]
  18. Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR. 18.  et al. 2012. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLOS Pathog. 8:10e1002940 [Google Scholar]
  19. Croll D, Ceresini P, Maciel J, McDonald BA. 19.  2016. The origin of wheat blast in Bangladesh. https://github.com/crolllab/wheat-blast
  20. Croll D, Lendenmann MH, Stewart E, McDonald BA. 20.  2015. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201:31213–28RADseq markers enabled identification of rapidly evolving recombination hot spots in two crosses of Zymoseptoria tritici. [Google Scholar]
  21. Croll D, McDonald BA. 21.  2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLOS Pathog. 8:e1002608 [Google Scholar]
  22. Croll D, Zala M, McDonald BA. 22.  2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLOS Genet. 9:6e1003567 [Google Scholar]
  23. Cumagun CJR, Bowden RL, Jurgenson JE, Leslie JF, Miedaner T. 23.  2004. Genetic mapping of pathogenicity and aggressiveness of Gibberella zeae (Fusarium graminearum) toward wheat. Phytopathology 94:5520–26 [Google Scholar]
  24. Dalman K, Himmelstrand K, Olson Å, Lind M, Brandström-Durling M, Stenlid J. 24.  2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLOS ONE 8:e53525 [Google Scholar]
  25. Davey JW, Blaxter ML. 25.  2010. RADseq: next-generation population genetics. Brief. Funct. Genom. 9:5–6416–23 [Google Scholar]
  26. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. 26.  2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12:7499–510Overview of methods for SNP genotyping by RADseq and GBS. [Google Scholar]
  27. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P. 27.  et al. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. PNAS 109:135110–15 [Google Scholar]
  28. de Jonge R, Bolton MD, Kombrink A, van den Berg GCM, Yadeta KA, Thomma BPHJ. 28.  2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23:81271–82 [Google Scholar]
  29. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR. 29.  et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43:5491–98 [Google Scholar]
  30. Ellegren H. 30.  2014. Genome sequencing and population genomics in non-model organisms. Trends Ecol. Evol. 29:151–63Excellent summary of the opportunities and challenges in population genomics for nonmodel organisms. [Google Scholar]
  31. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB. 31.  et al. 2011. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. PNAS 108:72831–36 [Google Scholar]
  32. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K. 32.  et al. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLOS ONE 6:5e19379 [Google Scholar]
  33. Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH. 33.  et al. 2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLOS Genet. 7:8e1002221 [Google Scholar]
  34. Frenkel O, Cadle-Davidson L, Wilcox WF, Milgroom MG. 34.  2015. Mechanisms of resistance to an azole fungicide in the grapevine powdery mildew fungus, Erysiphe necator. Phytopathology 105:3370–77 [Google Scholar]
  35. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H. 35.  et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38:8953–56 [Google Scholar]
  36. Gardiner DM, McDonald MC, Covarelli L, Solomon PS, Rusu AG. 36.  et al. 2012. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLOS Pathog. 8:9e1002952 [Google Scholar]
  37. Gire SK, Goba A, Andersen KG, Sealfon RSG, Park DJ. 37.  et al. 2014. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345:62021369–72 [Google Scholar]
  38. Goss EM, Cardenas ME, Myers K, Forbes GA, Fry WE. 38.  et al. 2011. The plant pathogen Phytophthora andina emerged via hybridization of an unknown Phytophthora species and the Irish potato famine pathogen, P. infestans. PLOS ONE 6:9e24543 [Google Scholar]
  39. Goss EM, Larsen M, Chastagner GA, Givens DR, Grünwald NJ. 39.  2009. Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLOS Pathog. 5:9e1000583 [Google Scholar]
  40. Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE. 40.  et al. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. PNAS 111:248791–96 [Google Scholar]
  41. Grünwald NJ, Flier WG. 41.  2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171–90 [Google Scholar]
  42. Grünwald NJ, Goss EM. 42.  2011. Evolution and population genetics of exotic and re-emerging pathogens: novel tools and approaches. Annu. Rev. Phytopathol. 49:249–67 [Google Scholar]
  43. Haas BJ, Kamoun S, O’Neill MC, Jiang RHY, Handsaker RE. 43.  et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:7262393–98 [Google Scholar]
  44. Hartl DL, Clark AG. 44.  2007. Principles of Population Genetics Sunderland, MA: Sinauer Assoc652, 4th ed.. [Google Scholar]
  45. Hemelaar J, Gouws E, Ghys PD, Osmanov S. 45.  2011. Global trends in molecular epidemiology of HIV-1 during 2000–2007. AIDS 25:5679–89 [Google Scholar]
  46. Ioos R, Andrieux A, Marçais B, Frey P. 46.  2006. Genetic characterization of the natural hybrid species Phytophthora alni as inferred from nuclear and mitochondrial DNA analyses. Fungal Genet. Biol. 43:7511–29 [Google Scholar]
  47. Kamvar ZN, Brooks JC, Grünwald NJ. 47.  2015. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6:208Significant extensions to the R package poppr for analyzing large, genome-wide SNP data in clonal organisms. [Google Scholar]
  48. Kamvar ZN, Tabima JF, Grünwald NJ. 48.  2014. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281 [Google Scholar]
  49. Kema GHJ, Goodwin SB, Hamza S, Verstappen ECP, Cavaletto JR. 49.  et al. 2002. A combined amplified fragment length polymorphism and randomly amplified polymorphism DNA genetic linkage map of Mycosphaerella graminicola, the Septoria tritici leaf blotch pathogen of wheat. Genetics 161:41497–505 [Google Scholar]
  50. Knaus BJ, Grünwald NJ. 50.  2016. VcfR: an R package to manipulate and visualize VCF format data. Mol. Ecol. Resour. In press [Google Scholar]
  51. Korte A, Farlow A. 51.  2013. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:129Excellent discussion of the biological and statistical considerations required for conducting GWASs. [Google Scholar]
  52. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P. 52.  2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12:1118–23 [Google Scholar]
  53. Langmead B, Salzberg SL. 53.  2012. Fast gapped–read alignment with Bowtie 2. Nature Methods 9:4357–59 [Google Scholar]
  54. Leinonen T, McCairns RJS, O’Hara RB, Merilä J. 54.  2013. QST-FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat. Rev. Genet. 14:3179–90 [Google Scholar]
  55. Lendenmann MH, Croll D, McDonald BA. 55.  2015. QTL mapping of fungicide sensitivity reveals novel genes and pleiotropy with melanization in the pathogen Zymoseptoria tritici. Fungal Genet. Biol. 80:53–67 [Google Scholar]
  56. Lendenmann MH, Croll D, Palma-Guerrero J, Stewart EL, McDonald BA. 56.  2016. QTL mapping of temperature sensitivity reveals candidate genes for thermal adaptation and growth morphology in the plant pathogenic fungus Zymoseptoria tritici. Heredity 116:4384–94 [Google Scholar]
  57. Lendenmann MH, Croll D, Stewart EL, McDonald BA. 57.  2014. Quantitative trait locus mapping of melanization in the plant pathogenic fungus Zymoseptoria tritici. G3 4:122519–33QTL analysis combining RADseq SNP markers with automated image analysis identified a candidate QTN affecting melanization in the PKS1 gene. [Google Scholar]
  58. Li H, Durbin R. 58.  2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:141754–60 [Google Scholar]
  59. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J. 59.  et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:162078–79 [Google Scholar]
  60. Li Y, Willer C, Sanna S, Abecasis G. 60.  2009. Genotype imputation. Annu. Rev. Genom. Hum. Genet. 10:387–406 [Google Scholar]
  61. Lind M, Dalman K, Stenlid J, Karlsson B, Olson Å. 61.  2007. Identification of quantitative trait loci affecting virulence in the basidiomycete Heterobasidion annosum s.l. Curr. Genet. 52:135–44 [Google Scholar]
  62. Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH. 62.  et al. 2013. Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLOS Genet. 9:1e1003215 [Google Scholar]
  63. Maciel JLN, Ceresini PC, Castroagudin VL, Zala M, Kema GHJ, McDonald BA. 63.  2014. Population structure and pathotype diversity of the wheat blast pathogen Magnaporthe oryzae 25 years after its emergence in Brazil. Phytopathology 104:195–107 [Google Scholar]
  64. Martin MD, Ho SYW, Wales N, Ristaino JB, Gilbert MTP. 64.  2014. Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant New World Phytophthora infestans. Mol. Biol. Evol. 31:61414–20 [Google Scholar]
  65. Martin MD, Vieira FG, Ho SYW, Wales N, Schubert M. 65.  et al. 2016. Genomic characterization of a South American Phytophthora hybrid mandates reassessment of the geographic origins of Phytophthora infestans. Mol. Biol. Evol. 33:2478–91 [Google Scholar]
  66. McDonald BA. 66.  2015. How can research on pathogen population biology suggest disease management strategies? The example of barley scald (Rhynchosporium commune). Plant Pathol. 64:51005–13 [Google Scholar]
  67. McDonald BA, Mundt CC. 67.  2016. How knowledge of pathogen population biology informs management of Septoria tritici blotch. Phytopathology http://dx.doi.org/10.1094/PHYTO-03-16-0131-RVW [Google Scholar]
  68. McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA. 68.  2013. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol. 199:1241–51 [Google Scholar]
  69. Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S. 69.  et al. 2016. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat. Genet. 48:2201–5 [Google Scholar]
  70. Milgroom MG. 70.  2015. Population Biology of Plant Pathogens: Genetics, Ecology, and Evolution St. Paul, MN: APS PressA comprehensive introduction to population genetics of fungi and oomycetes. [Google Scholar]
  71. Milgroom MG, Jiménez-Gasco MM, Olivares García C, Drott MT, Jiménez-Díaz RM. 71.  2014. Recombination between clonal lineages of the asexual fungus Verticillium dahliae detected by genotyping by sequencing. PLOS ONE 9:9e106740 [Google Scholar]
  72. Milgroom MG, Jiménez-Gasco MM, Olivares-García C, Jiménez-Díaz RM. 72.  2016. Clonal expansion and migration of a highly virulent, defoliating lineage of Verticillium dahliae. Phytopathology http://dx.doi.org/10.1094/PHYTO-11-15-0300-R [Google Scholar]
  73. Nielsen R. 73.  2005. Molecular signatures of natural selection. Annu. Rev. Genet. 39:197–218 [Google Scholar]
  74. Otter JA, French GL. 74.  2010. Molecular epidemiology of community-associated methicillin-resistant Staphylococcus aureus in Europe. Lancet Infect. Dis. 10:4227–39 [Google Scholar]
  75. Poppe S, Dorsheimer L, Happel P, Stukenbrock EH. 75.  2015. Rapidly evolving genes are key players in host specialization and virulence of the fungal wheat pathogen Zymoseptoria tritici (Mycosphaerella graminicola). PLOS Pathog. 11:7e1005055 [Google Scholar]
  76. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D. 76.  et al. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:60101540–43 [Google Scholar]
  77. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ. 77.  2006. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16:181857–64 [Google Scholar]
  78. Salamini F, Ozkan H, Brandolini A, Schäfer-Pregl R, Martin W. 78.  2002. Genetics and geography of wild cereal domestication in the Near East. Nat. Rev. Genet. 3:6429–41 [Google Scholar]
  79. Schmidt SM, Lukasiewicz J, Farrer R, van Dam P, Bertoldo C, Rep M. 79.  2016. Comparative genomics of Fusarium oxysporum f. sp. melonis reveals the secreted protein recognized by the fom-2 resistance gene in melon. New Phytol. 209:1307–18 [Google Scholar]
  80. Short DPG, Gurung S, Hu X, Inderbitzin P, Subbarao KV. 80.  2014. Maintenance of sex-related genes and the co-occurrence of both mating types in Verticillium dahliae. PLOS ONE 9:11e112145 [Google Scholar]
  81. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM. 81.  et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:60101543–46 [Google Scholar]
  82. Stefansson TS, Willi Y, Croll D, McDonald BA. 82.  2014. An assay for quantitative virulence in Rhynchosporium commune reveals an association between effector genotype and virulence. Plant Pathol. 63:2405–14 [Google Scholar]
  83. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE et al.83.  2016. QTL mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici. bioRxiv. http://dx.doi.org/10.1101/051169
  84. Stewart EL, McDonald BA. 84.  2014. Measuring quantitative virulence in the wheat pathogen Zymoseptoria tritici using high-throughput automated image analysis. Phytopathology 104:9985–92 [Google Scholar]
  85. Stinchcombe J, Hoekstra H. 85.  2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:2158–70 [Google Scholar]
  86. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA. 86.  2007. Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol. Biol. Evol. 24:2398–411 [Google Scholar]
  87. Stukenbrock EH, Bataillon T. 87.  2012. A population genomics perspective on the emergence and adaptation of new plant pathogens in agro-ecosystems. PLOS Pathog. 8:9e1002893 [Google Scholar]
  88. Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R. 88.  et al. 2011. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Res. 21:122157–66Comparative population genomics analysis illustrating several analytical methods to identify candidate genes involved in host specialization and speciation. [Google Scholar]
  89. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 89.  2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. PNAS 109:2710954–59 [Google Scholar]
  90. Stukenbrock EH, Croll D. 90.  2014. The evolving fungal genome. Fungal Biol. Rev. 28:11–12 [Google Scholar]
  91. Stukenbrock EH, McDonald BA. 91.  2009. Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol. Plant-Microbe Interact. 22:371–80 [Google Scholar]
  92. Talas F, Kalih R, Miedaner T, McDonald BA. 92.  2016. Genome-wide association study identifies novel candidate genes for aggressiveness, deoxynivalenol production, and azole sensitivity in natural field populations of Fusarium graminearum. Mol. Plant-Microbe Interact. 29417–30 [Google Scholar]
  93. Talas F, McDonald BA. 93.  2015. Genome-wide analysis of Fusarium graminearum field populations reveals hotspots of recombination. BMC Genom. 16:996 [Google Scholar]
  94. Torriani SFF, Brunner PC, McDonald BA. 94.  2011. Evolutionary history of the mitochondrial genome in Mycosphaerella populations infecting bread wheat, durum wheat and wild grasses. Mol. Phylogenet. Evol. 58:2192–97 [Google Scholar]
  95. Torriani SF, Brunner PC, McDonald BA, Sierotzki H. 95.  2009. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag. Sci. 65:2155–62 [Google Scholar]
  96. Torriani SFF, Goodwin SB, Kema GHJ, Pangilinan JL, McDonald BA. 96.  2008. Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet. Biol. 45:5628–37 [Google Scholar]
  97. Torriani SFF, Penselin D, Knogge W, Felder M, Taudien S. 97.  et al. 2014. Comparative analysis of mitochondrial genomes from closely related Rhynchosporium species reveals extensive intron invasion. Fungal Genet. Biol. 62:34–42 [Google Scholar]
  98. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY. 98.  et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:57911261–66 [Google Scholar]
  99. Van de Wouw AP, Marcroft SJ, Ware A, Lindbeck K, Khangura R, Howlett BJ. 99.  2014. Breakdown of resistance to the fungal disease, blackleg, is averted in commercial canola (Brassica napus) crops in Australia. Field Crops Res. 166:144–51 [Google Scholar]
  100. Vinatzer BA, Monteil CL, Clarke CR. 100.  2014. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu. Rev. Phytopathol. 52:19–43 [Google Scholar]
  101. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R. 101.  et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49:507–31 [Google Scholar]
  102. Walker AS, Bouguennec A, Confais J, Morgant G, Leroux P. 102.  2011. Evidence of host-range expansion from new powdery mildew (Blumeria graminis) infections of triticale (×Triticosecale) in France. Plant Pathol. 60:2207–20 [Google Scholar]
  103. Weigel D, Nordborg M. 103.  2015. Population genomics for understanding adaptation in wild plant species. Annu. Rev. Genet. 49:315–38An excellent introduction to population genomics oriented mainly around plants, particularly Arabidopsis. [Google Scholar]
  104. Wolfe MS, McDermott JM. 104.  1994. Population genetics of plant pathogen interactions: the example of the Erysiphe graminis–Hordeum vulgare pathosystem. Annu. Rev. Phytopathol. 32:89–113 [Google Scholar]
  105. Wooley JC, Godzik A, Friedberg I. 105.  2010. A primer on metagenomics. PLOS Comput. Biol. 6:2e1000667 [Google Scholar]
  106. Zhu C, Gore M, Buckler ES, Yu J. 106.  2008. Status and prospects of association mapping in plants. Plant Genome 1:15 [Google Scholar]
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