Population Genomics of Fungal and Oomycete Pathogens

Annual Review of Phytopathology

Volumn 54, Issue , 2016, Pages 323-346

  Grünwald, Niklaus J ^a,b,d   McDonald, Bruce A ^c   Milgroom, Michael G ^d  

^a HORTICULTURAL CROPS RESEARCH LABORATORY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c ETH ZURICH   (Switzerland)

^d Department of Obstetrics Gynecology   (United States)

Author keywords

Adaptation; Comparative genomics; Evolution; Genome wide association; Population genetics; QTL mapping

Indexed keywords

FUNGAL GENOME; FUNGUS; GENETICS; GENOMICS; MICROBIOLOGY; OOMYCETES; PHYSIOLOGY; PLANT; PLANT DISEASE;

FUNGI; GENOME, FUNGAL; GENOMICS; OOMYCETES; PLANT DISEASES; PLANTS;

EID: 84981351774     PISSN: 00664286     EISSN: 15452107     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-080614-115913     Document Type: Review

References (106)

1. Aguileta G, Refrégier G, Yockteng R, Fournier E, Giraud T. 2009. Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect. Genet. Evol. 9(4):656-70
2. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. 2016. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat. Rev. Genet. 17(2):81-92
3. Andrews KR, Luikart G. 2014. Recent novel approaches for population genomics data analysis. Mol. Ecol. 23(7):1661-67
4. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, et al. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLOS ONE 3(10):e3376
5. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633-35
6. Browning BL, Browning SR. 2016. Genotype imputation with millions of reference samples. Am. J. Hum. Genet. 98(1):116-26
7. Browning SR. 2008. Missing data imputation and haplotype phase inference for genome-wide association studies. Hum. Genet. 124(5):439-50
8. Browning SR, Browning BL. 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(5):1084-97
9. Browning SR, Browning BL. 2011. Haplotype phasing: existing methods and new developments. Nat. Rev. Genet. 12(10):703-14
10. Brunner PC, Stefanato FL, McDonald BA. 2008. Evolution of the CYP51 gene in Mycosphaerella graminicola: evidence for intragenic recombination and selective replacement. Mol. Plant Pathol. 9(3):305-16
11. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA. 2013. Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen. Mol. Biol. Evol. 30(6):1337-47
12. Brunner PC, Torriani SFF, Croll D, Stukenbrock EH, McDonald BA. 2014. Hitchhiking selection is driving intron gain in a pathogenic fungus. Mol. Biol. Evol. 31(7):1741-49
13. Callaway E. 2016. Devastating wheat fungus appears in Asia for first time. Nature 532:421-22
14. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The carbohydrateactive enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37:D233-38
15. Castroagudín VL, Ceresini PC, de Oliveira SC, Reges JTA, Maciel JLN, et al. 2015. Resistance to QoI fungicides is widespread in Brazilian populations of the wheat blast pathogen Magnaporthe oryzae. Phytopathology 105(3):284-94
16. Castroagudín VL, Moreira SI, Pereira DAS, Moreira SS, Brunner PC, et al. 2016. Pyricularia graministritici sp. nov., a new Pyricularia species causing wheat blast. Persoonia. In press
17. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH, DeKoning D-J. 2011. Stacks: building and genotyping loci de novo from short-read sequences. G3 1(3):171-82
18. Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, et al. 2012. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLOS Pathog. 8(10):e1002940
19. Croll D, Ceresini P, Maciel J, McDonald BA. 2016. The origin of wheat blast in Bangladesh. https://github.com/crolllab/wheat-blast
20. Croll D, Lendenmann MH, Stewart E, McDonald BA. 2015. The impact of recombination hotspots on genome evolution of a fungal plant pathogen. Genetics 201(3):1213-28
21. Croll D, McDonald BA. 2012. The accessory genome as a cradle for adaptive evolution in pathogens. PLOS Pathog. 8:e1002608
22. Croll D, Zala M, McDonald BA. 2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLOS Genet. 9(6):e1003567
23. Cumagun CJR, Bowden RL, Jurgenson JE, Leslie JF, Miedaner T. 2004. Geneticmapping of pathogenicity and aggressiveness of Gibberella zeae (Fusarium graminearum) toward wheat. Phytopathology 94(5):520-26
24. Dalman K, Himmelstrand K, Olson Å, Lind M, Brandström-Durling M, Stenlid J. 2013. A genomewide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLOS ONE 8:e53525
25. Davey JW, Blaxter ML. 2010. RADseq: next-generation population genetics. Brief. Funct. Genom. 9(5-6):416-23
26. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. 2011. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat. Rev. Genet. 12(7):499-510
27. de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, et al. 2012. Tomato immune receptor Ve1 recognizes effector ofmultiple fungal pathogens uncovered by genome and RNA sequencing. PNAS 109(13):5110-15
28. de Jonge R, Bolton MD, Kombrink A, van den Berg GCM, Yadeta KA, Thomma BPHJ. 2013. Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res. 23(8):1271-82
29. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43(5):491-98
30. Ellegren H. 2014. Genome sequencing and population genomics in non-model organisms. Trends Ecol. Evol. 29(1):51-63
31. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, et al. 2011. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. PNAS 108(7):2831-36
32. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, et al. 2011. A robust, simple genotyping-bysequencing (GBS) approach for high diversity species. PLOS ONE 6(5):e19379
33. Famoso AN, Zhao K, Clark RT, Tung C-W, Wright MH, et al. 2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QT Lmapping. PLOS Genet. 7(8):e1002221
34. Frenkel O, Cadle-Davidson L, Wilcox WF, Milgroom MG. 2015. Mechanisms of resistance to an azole fungicide in the grapevine powdery mildew fungus, Erysiphe necator. Phytopathology 105(3):370-77
35. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat. Genet. 38(8):953-56
36. Gardiner DM, McDonald MC, Covarelli L, Solomon PS, Rusu AG, et al. 2012. Comparative pathogenomics reveals horizontally acquired novel virulence genes in fungi infecting cereal hosts. PLOS Pathog. 8(9):e1002952
37. Gire SK, Goba A, Andersen KG, Sealfon RSG, Park DJ, et al. 2014. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345(6202):1369-72
38. Goss EM, Cardenas ME, Myers K, Forbes GA, Fry WE, 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(9):e24543
39. Goss EM, Larsen M, Chastagner GA, Givens DR, Grünwald NJ. 2009. Population genetic analysis infers migration pathways of Phytophthora ramorum in US nurseries. PLOS Pathog. 5(9):e1000583
40. Goss EM, Tabima JF, Cooke DEL, Restrepo S, Fry WE, et al. 2014. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. PNAS 111(24):8791-96
41. Grünwald NJ, Flier WG. 2005. The biology of Phytophthora infestans at its center of origin. Annu. Rev. Phytopathol. 43:171-90
42. Grünwald NJ, Goss EM. 2011. Evolution and population genetics of exotic and re-emerging pathogens: novel tools and approaches. Annu. Rev. Phytopathol. 49:249-67
43. Haas BJ, Kamoun S, O'Neill MC, Jiang RHY, Handsaker RE, et al. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461(7262):393-98
44. Hartl DL, Clark AG. 2007. Principles of Population Genetics. Sunderland, MA: Sinauer Assoc. 652 pp. 4th ed.
45. Hemelaar J, Gouws E, Ghys PD, Osmanov S. 2011. Global trends in molecular epidemiology of HIV-1 during 2000-2007. AIDS 25(5):679-89
46. Ioos R, Andrieux A, Marçais B, Frey P. 2006. Genetic characterization of the natural hybrid species Phytophthora alni as inferred from nuclear and mitochondrial DNA analyses. Fungal Genet. Biol. 43(7):511-29
47. Kamvar ZN, Brooks JC, Grünwald NJ. 2015. Novel R tools for analysis of genome-wide population genetic data with emphasis on clonality. Front. Genet. 6:208
48. Kamvar ZN, Tabima JF, Grünwald NJ. 2014. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. Peer J 2:e281
49. Kema GHJ, Goodwin SB, Hamza S, Verstappen ECP, Cavaletto JR, 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(4):1497-505
50. Knaus BJ, Grünwald NJ 2016. VcfR: an R package to manipulate and visualize VCF format data. Mol. Ecol. Resour. In press
51. Korte A, Farlow A. 2013. The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9(1):29
52. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P. 2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12(1):118-23
53. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9(4):357-59
54. ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat. Rev. Genet. 14(3):179-90
55. Lendenmann MH, Croll D, McDonald BA. 2015. QTL mapping of fungicide sensitivity reveals novel genes and pleiotropy with melanization in the pathogen Zymoseptoria tritici. Fungal Genet. Biol. 80:53-67
56. Lendenmann MH, Croll D, Palma-Guerrero J, Stewart EL, McDonald BA. 2016. QTL mapping of temperature sensitivity reveals candidate genes for thermal adaptation and growth morphology in the plant pathogenic fungus Zymoseptoria tritici. Heredity 116(4):384-94
57. Lendenmann MH, Croll D, Stewart EL, McDonald BA. 2014. Quantitative trait locus mapping of melanization in the plant pathogenic fungus Zymoseptoria tritici. G3 4(12):2519-33
58. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754-60
59. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078-79
60. Li Y, Willer C, Sanna S, Abecasis G. 2009. Genotype imputation. Annu. Rev. Genom. Hum. Genet. 10:387-406
61. Lind M, Dalman K, Stenlid J, Karlsson B, Olson Å. 2007. Identification of quantitative trait loci affecting virulence in the basidiomycete Heterobasidion annosum s.l. Curr. Genet. 52(1):35-44
62. Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, et al. 2013. Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLOS Genet. 9(1):e1003215
63. Maciel JLN, Ceresini PC, Castroagudin VL, Zala M, Kema GHJ, McDonald BA. 2014. Population structure and pathotype diversity of the wheat blast pathogen Magnaporthe oryzae 25 years after its emergence in Brazil. Phytopathology 104(1):95-107
64. Martin MD, Ho SYW, Wales N, Ristaino JB, Gilbert MTP. 2014. Persistence of the mitochondrial lineage responsible for the Irish potato famine in extant New World Phytophthora infestans. Mol. Biol. Evol. 31(6):1414-20
65. Martin MD, Vieira FG, Ho SYW, Wales N, Schubert M, et al. 2016. Genomic characterization of a South American Phytophthora hybrid mandates reassessment of the geographic origins of Phytophthora infestans. Mol. Biol. Evol. 33(2):478-91
66. McDonald BA. 2015. How can research on pathogen population biology suggest disease management strategies? The example of barley scald (Rhynchosporium commune). Plant Pathol. 64(5):1005-13
67. McDonald BA, Mundt CC. 2016. How knowledge of pathogen population biology informsmanagement of Septoria tritici blotch. Phytopathology http://dx.doi.org/10.1094/PHYTO-03-16-0131-RVW
68. McDonald MC, Oliver RP, Friesen TL, Brunner PC, McDonald BA. 2013. Global diversity and distribution of three necrotrophic effectors in Phaeosphaeria nodorum and related species. New Phytol. 199(1):241-51
69. Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, et al. 2016. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat. Genet. 48(2):201-5
70. Milgroom MG. 2015. Population Biology of Plant Pathogens: Genetics, Ecology, and Evolution. St. Paul, MN: APS Press
71. Milgroom MG, Jiménez-Gasco MM, Olivares García C, Drott MT, Jiménez-Díaz RM. 2014. Recombination between clonal lineages of the asexual fungus Verticillium dahliae detected by genotyping by sequencing. PLOS ONE 9(9):e106740
72. Milgroom MG, Jiménez-Gasco MM, Olivares-García C, Jiménez-Díaz RM. 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
73. Nielsen R. 2005. Molecular signatures of natural selection. Annu. Rev. Genet. 39:197-218
74. Otter JA, French GL. 2010. Molecular epidemiology of community-associated methicillin-resistant Staphylococcus aureus in Europe. Lancet Infect. Dis. 10(4):227-39
75. Poppe S, Dorsheimer L, Happel P, Stukenbrock EH. 2015. Rapidly evolving genes are key players in host specialization and virulence of the fungal wheat pathogen Zymoseptoria tritici (Mycosphaerella graminicola). PLOS Pathog. 11(7):e1005055
76. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, et al. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330(6010):1540-43
77. Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ. 2006. Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr. Biol. 16(18):1857-64
78. Salamini F, Ozkan H, Brandolini A, Schäfer-Pregl R, Martin W. 2002. Genetics and geography of wild cereal domestication in the Near East. Nat. Rev. Genet. 3(6):429-41
79. Schmidt SM, Lukasiewicz J, Farrer R, van Dam P, Bertoldo C, Rep M. 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(1):307-18
80. Short DPG, Gurung S, Hu X, Inderbitzin P, Subbarao KV. 2014. Maintenance of sex-related genes and the co-occurrence of both mating types in Verticillium dahliae. PLOS ONE 9(11):e112145
81. Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330(6010):1543-46
82. Stefansson TS, Willi Y, Croll D, McDonald BA. 2014. An assay for quantitative virulence in Rhynchosporium commune reveals an association between effector genotype and virulence. Plant Pathol. 63(2):405-14
83. Stewart EL, Croll D, Lendenmann MH, Sanchez-Vallet A, Hartmann FE, et al. 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. 2014. Measuring quantitative virulence in the wheat pathogen Zymoseptoria tritici using high-throughput automated image analysis. Phytopathology 104(9):985-92
85. Stinchcombe J, Hoekstra H. 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100(2):158-70
86. Stukenbrock EH, Banke S, Javan-Nikkhah M, McDonald BA. 2007. Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Mol. Biol. Evol. 24(2):398-411
87. Stukenbrock EH, Bataillon T. 2012. Apopulation genomics perspective on the emergence and adaptation of new plant pathogens in agro-ecosystems. PLOS Pathog. 8(9):e1002893
88. Stukenbrock EH, Bataillon T, Dutheil JY, Hansen TT, Li R, 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(12):2157-66
89. Stukenbrock EH, Christiansen FB, Hansen TT, Dutheil JY, Schierup MH. 2012. Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species. PNAS 109(27):10954-59
90. Stukenbrock EH, Croll D. 2014. The evolving fungal genome. Fungal Biol. Rev. 28(1):1-12
91. Stukenbrock EH, McDonald BA. 2009. Population genetics of fungal and oomycete effectors involved in gene-for-gene interactions. Mol. Plant-Microbe Interact. 22:371-80
92. Talas F, Kalih R, Miedaner T, McDonald BA. 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. 29:417-30
93. Talas F, McDonald BA. 2015. Genome-wide analysis of Fusarium graminearum field populations reveals hotspots of recombination. BMC Genom. 16:996
94. Torriani SFF, Brunner PC, McDonald BA. 2011. Evolutionary history of the mitochondrial genome in Mycosphaerella populations infecting bread wheat, durum wheat and wild grasses. Mol. Phylogenet. Evol. 58(2):192-97
95. Torriani SF, Brunner PC, McDonald BA, Sierotzki H. 2009. QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag. Sci. 65(2):155-62
96. Torriani SFF, Goodwin SB, Kema GHJ, Pangilinan JL, McDonald BA. 2008. Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet. Biol. 45(5):628-37
97. Torriani SFF, Penselin D, Knogge W, Felder M, Taudien S, et al. 2014. Comparative analysis of mitochondrial genomes from closely related Rhynchosporium species reveals extensive intron invasion. Fungal Genet. Biol. 62:34-42
98. Tyler BM, Tripathy S, Zhang X, Dehal P, Jiang RHY, et al. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313(5791):1261-66
99. Van de Wouw AP, Marcroft SJ, Ware A, Lindbeck K, Khangura R, Howlett BJ. 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
100. Vinatzer BA, Monteil CL, Clarke CR. 2014. Harnessing population genomics to understand how bacterial pathogens emerge, adapt to crop hosts, and disseminate. Annu. Rev. Phytopathol. 52:19-43
101. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, et al. 2011. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 49:507-31
102. Walker AS, Bouguennec A, Confais J, Morgant G, Leroux P. 2011. Evidence of host-range expansion from new powdery mildew (Blumeria graminis) infections of triticale (×Triticosecale) in France. Plant Pathol. 60(2):207-20
103. Weigel D, Nordborg M. 2015. Population genomics for understanding adaptation in wild plant species. Annu. Rev. Genet. 49:315-38
104. Wolfe MS, McDermott JM. 1994. Population genetics of plant pathogen interactions: the example of the Erysiphe graminis-Hordeum vulgare pathosystem. Annu. Rev. Phytopathol. 32:89-113
105. Wooley JC, Godzik A, Friedberg I. 2010. A primer onmetagenomics. PLOS Comput. Biol. 6(2):e1000667
106. Zhu C, Gore M, Buckler ES, Yu J. 2008. Status and prospects of association mapping in plants. Plant Genome 1(1):5