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Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity

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  • Authors: John W. Taylor1, Sara Branco2, Cheng Gao3, Chris Hann-Soden4, Liliam Montoya5, Iman Sylvain6, Pierre Gladieux7
  • Editors: Joseph Heitman8, Eva Holtgrewe Stukenbrock9
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Plant and Microbial Biology, University of California, Berkeley, CA, 94720-3102; 2: Département Génétique et Ecologie Evolutives Laboratoire Ecologie, Systématique et Evolution, CNRS-UPS-AgroParisTech, Université de Paris-Sud, 91405 Orsay, France, and Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717; 3: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102; 4: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102; 5: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102; 6: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102; 7: INRA, UMR BGPI, Campus International de Baillarguet, 34398 Montpellier, France; 8: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 9: Environmental Genomics, Christian-Albrechts University of Kiel, Kiel, Germany, and Max Planck Institute for Evolutionary Biology, Plön, Germany
    • Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0057-2016
  • Received 13 June 2017 Accepted 03 July 2017 Published 22 September 2017
  • John W. Taylor, [email protected]
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  • Abstract:

    The first eukaryotic genome to be sequenced was fungal, and there continue to be more sequenced genomes in the kingdom Fungi than in any other eukaryotic kingdom. Comparison of these genomes reveals many sources of genetic variation, from single nucleotide polymorphisms to horizontal gene transfer and on to changes in the arrangement and number of chromosomes, not to mention endofungal bacteria and viruses. Population genomics shows that all sources generate variation all the time and implicate natural selection as the force maintaining genome stability. Variation in wild populations is a rich resource for associating genetic variation with phenotypic variation, whether through quantitative trait locus mapping, genome-wide association studies, or reverse ecology. Subjects of studies associating genetic and phenotypic variation include model fungi, e.g., and , but pioneering studies have also been made with fungi pathogenic to plants, e.g., (= ), , and , and to humans, e.g., , , and .

  • Citation: Taylor J, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, Gladieux P. 2017. Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity. Microbiol Spectrum 5(5):FUNK-0057-2016. doi:10.1128/microbiolspec.FUNK-0057-2016.

References

1. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG. 1996. Life with 6000 genes. Science 274:546–567 http://dx.doi.org/10.1126/science.274.5287.546. [PubMed]
2. Galagan JE, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868 http://dx.doi.org/10.1038/nature01554. [PubMed]
3. Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D. 2004. Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700 http://dx.doi.org/10.1038/nbt967. [PubMed]
4. Machida M, et al. 2005. Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161 http://dx.doi.org/10.1038/nature04300. [PubMed]
5. Nierman WC, et al. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156 http://dx.doi.org/10.1038/nature04332. [PubMed]
6. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Baştürkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Peñalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW. 2005. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115 http://dx.doi.org/10.1038/nature04341. [PubMed]
7. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES. 2003. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423:241–254 http://dx.doi.org/10.1038/nature01644. [PubMed]
8. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713 http://dx.doi.org/10.1038/42711. [PubMed]
9. Llorente B, Malpertuy A, Neuvéglise C, de Montigny J, Aigle M, Artiguenave F, Blandin G, Bolotin-Fukuhara M, Bon E, Brottier P, Casaregola S, Durrens P, Gaillardin C, Lépingle A, Ozier-Kalogéropoulos O, Potier S, Saurin W, Tekaia F, Toffano-Nioche C, Wésolowski-Louvel M, Wincker P, Weissenbach J, Souciet J, Dujon B. 2000. Genomic exploration of the hemiascomycetous yeasts. 18. Comparative analysis of chromosome maps and synteny with Saccharomyces cerevisiae. FEBS Lett 487:101–112 http://dx.doi.org/10.1016/S0014-5793(00)02289-4.
10. Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pöhlmann R, Luedi P, Choi S, Wing RA, Flavier A, Gaffney TD, Philippsen P. 2004. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science 304:304–307 http://dx.doi.org/10.1126/science.1095781. [PubMed]
11. Kellis M, Birren BW, Lander ES. 2004. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428:617–624 http://dx.doi.org/10.1038/nature02424. [PubMed]
12. Marcet-Houben M, Gabaldón T. 2015. Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker’s yeast lineage. PLoS Biol 13:e1002220 http://dx.doi.org/10.1371/journal.pbio.1002220. [PubMed]
13. Wolfe KH. 2015. Origin of the yeast whole-genome duplication. PLoS Biol 13:e1002221 http://dx.doi.org/10.1371/journal.pbio.1002221. [PubMed]
14. Koszul R, Caburet S, Dujon B, Fischer G. 2004. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J 23:234–243 http://dx.doi.org/10.1038/sj.emboj.7600024. [PubMed]
15. Koszul R, Dujon B, Fischer G. 2006. Stability of large segmental duplications in the yeast genome. Genetics 172:2211–2222 http://dx.doi.org/10.1534/genetics.105.048058. [PubMed]
16. Wapinski I, Pfeffer A, Friedman N, Regev A. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61 http://dx.doi.org/10.1038/nature06107. [PubMed]
17. Assis R, Bachtrog D. 2013. Neofunctionalization of young duplicate genes in Drosophila. Proc Natl Acad Sci USA 110:17409–17414 http://dx.doi.org/10.1073/pnas.1313759110. [PubMed]
18. Daverdin G, Rouxel T, Gout L, Aubertot J-N, Fudal I, Meyer M, Parlange F, Carpezat J, Balesdent M-H. 2012. Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog 8:e1003020 http://dx.doi.org/10.1371/journal.ppat.1003020. [PubMed]
19. Hartmann FE, Sánchez-Vallet A, McDonald BA, Croll D. 2017. A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements. ISME J 11:1189–1204 http://dx.doi.org/10.1038/ismej.2016.196. [PubMed]
20. Lespinet O, Wolf YI, Koonin EV, Aravind L. 2002. The role of lineage-specific gene family expansion in the evolution of eukaryotes. Genome Res 12:1048–1059 http://dx.doi.org/10.1101/gr.174302. [PubMed]
21. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW. 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986 http://dx.doi.org/10.1038/nature03449. [PubMed]
22. Soanes DM, Alam I, Cornell M, Wong HM, Hedeler C, Paton NW, Rattray M, Hubbard SJ, Oliver SG, Talbot NJ. 2008. Comparative genome analysis of filamentous fungi reveals gene family expansions associated with fungal pathogenesis. PLoS One 3:e2300 http://dx.doi.org/10.1371/journal.pone.0002300. [PubMed]
23. Hahn MW, De Bie T, Stajich JE, Nguyen C, Cristianini N. 2005. Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome Res 15:1153–1160 http://dx.doi.org/10.1101/gr.3567505. [PubMed]
24. Sharpton TJ, Stajich JE, Rounsley SD, Gardner MJ, Wortman JR, Jordar VS, Maiti R, Kodira CD, Neafsey DE, Zeng Q, Hung CY, McMahan C, Muszewska A, Grynberg M, Mandel MA, Kellner EM, Barker BM, Galgiani JN, Orbach MJ, Kirkland TN, Cole GT, Henn MR, Birren BW, Taylor JW. 2009. Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res 19:1722–1731 http://dx.doi.org/10.1101/gr.087551.108. [PubMed]
25. Floudas D, et al. 2012. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719 http://dx.doi.org/10.1126/science.1221748. [PubMed]
26. Whiston E, Taylor JW. 2016. Comparative phylogenomics of pathogenic and nonpathogenic species. G3 (Bethesda) 6:235–244 http://dx.doi.org/10.1534/g3.115.022806. [PubMed]
27. Rosewich UL, Kistler HC. 2000. Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38:325–363 http://dx.doi.org/10.1146/annurev.phyto.38.1.325. [PubMed]
28. Garcia-Vallvé S, Romeu A, Palau J. 2000. Horizontal gene transfer of glycosyl hydrolases of the rumen fungi. Mol Biol Evol 17:352–361 http://dx.doi.org/10.1093/oxfordjournals.molbev.a026315. [PubMed]
29. Fitzpatrick DA. 2012. Horizontal gene transfer in fungi. FEMS Microbiol Lett 329:1–8 http://dx.doi.org/10.1111/j.1574-6968.2011.02465.x. [PubMed]
30. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ. 2009. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 21:1897–1911 http://dx.doi.org/10.1105/tpc.109.065805. [PubMed]
31. Richards TA, Soanes DM, Jones MDM, Vasieva O, Leonard G, Paszkiewicz K, Foster PG, Hall N, Talbot NJ. 2011. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci USA 108:15258–15263 http://dx.doi.org/10.1073/pnas.1105100108. [PubMed]
32. Wang Y, White MM, Kvist S, Moncalvo J-M. 2016. Genome-wide survey of gut fungi (Harpellales) reveals the first horizontally transferred ubiquitin gene from a mosquito host. Mol Biol Evol 33:2544–2554 http://dx.doi.org/10.1093/molbev/msw126. [PubMed]
33. Castanera R, Borgognone A, Pisabarro AG, Ramírez L. 2017. Biology, dynamics, and applications of transposable elements in basidiomycete fungi. Appl Microbiol Biotechnol 101:1337–1350 http://dx.doi.org/10.1007/s00253-017-8097-8. [PubMed]
34. Daboussi MJ, Davière JM, Graziani S, Langin T. 2002. Evolution of the Fot1 transposons in the genus Fusarium: discontinuous distribution and epigenetic inactivation. Mol Biol Evol 19:510–520 http://dx.doi.org/10.1093/oxfordjournals.molbev.a004106. [PubMed]
35. Muszewska A, Hoffman-Sommer M, Grynberg M. 2011. LTR retrotransposons in fungi. PLoS One 6:e29425 http://dx.doi.org/10.1371/journal.pone.0029425. [PubMed]
36. Selker EU. 2002. Repeat-induced gene silencing in fungi. Adv Genet 46:439–450 http://dx.doi.org/10.1016/S0065-2660(02)46016-6.
37. Hane JK, Williams AH, Taranto AP, Solomon PS, Oliver RP. 2015. Repeat-induced point mutation: a fungal-specific, endogenous mutagenesis process, p 55–68. In van den Berg MA, Maruthachalam K (ed), Genetic Transformation Systems in Fungi, vol 2. Springer International Publishing, Cham, Switzerland http://dx.doi.org/10.1007/978-3-319-10503-1_4.
38. Raffaele S, Kamoun S. 2012. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10:417–430.
39. Horns F, Petit E, Hood ME. 2017. Massive expansion of Gypsy-like retrotransposons in Microbotryum fungi. Genome Biol Evol 9:363–371 http://dx.doi.org/10.1093/gbe/evx011. [PubMed]
40. Vanheule A, Audenaert K, Warris S, van de Geest H, Schijlen E, Höfte M, De Saeger S, Haesaert G, Waalwijk C, van der Lee T. 2016. Living apart together: crosstalk between the core and supernumerary genomes in a fungal plant pathogen. BMC Genomics 17:670 http://dx.doi.org/10.1186/s12864-016-2941-6. [PubMed]
41. Goddard MR, Burt A. 1999. Recurrent invasion and extinction of a selfish gene. Proc Natl Acad Sci USA 96:13880–13885 http://dx.doi.org/10.1073/pnas.96.24.13880. [PubMed]
42. Koufopanou V, Goddard MR, Burt A. 2002. Adaptation for horizontal transfer in a homing endonuclease. Mol Biol Evol 19:239–246 http://dx.doi.org/10.1093/oxfordjournals.molbev.a004077. [PubMed]
43. Burt A. 2003. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc Biol Sci 270:921–928 http://dx.doi.org/10.1098/rspb.2002.2319. [PubMed]
44. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821 http://dx.doi.org/10.1126/science.1225829. [PubMed]
45. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956 http://dx.doi.org/10.1038/ng1839. [PubMed]
46. Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci USA 107:13544–13549 http://dx.doi.org/10.1073/pnas.1004090107. [PubMed]
47. Shi G, Zhang Z, Friesen TL, Raats D, Fahima T, Brueggeman RS, Lu S, Trick HN, Liu Z, Chao W, Frenkel Z, Xu SS, Rasmussen JB, Faris JD. 2016. The hijacking of a receptor kinase-driven pathway by a wheat fungal pathogen leads to disease. Sci Adv 2:e1600822 http://dx.doi.org/10.1126/sciadv.1600822. [PubMed]
48. Lorang JM, Sweat TA, Wolpert TJ. 2007. Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci USA 104:14861–14866 http://dx.doi.org/10.1073/pnas.0702572104. [PubMed]
49. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG. 2003. Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci USA 100:15670–15675 http://dx.doi.org/10.1073/pnas.2532165100. [PubMed]
50. Keller NP, Turner G, Bennett JW. 2005. Fungal secondary metabolism - from biochemistry to genomics. Nat Rev Microbiol 3:937–947 http://dx.doi.org/10.1038/nrmicro1286. [PubMed]
51. Walton JD. 2000. Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30:167–171 http://dx.doi.org/10.1006/fgbi.2000.1224. [PubMed]
52. Ropars J, Rodríguez de la Vega RC, López-Villavicencio M, Gouzy J, Sallet E, Dumas É, Lacoste S, Debuchy R, Dupont J, Branca A, Giraud T. 2015. Adaptive horizontal gene transfers between multiple cheese-associated fungi. Curr Biol 25:2562–2569 http://dx.doi.org/10.1016/j.cub.2015.08.025. [PubMed]
53. Cheeseman K, Ropars J, Renault P, Dupont J, Gouzy J, Branca A, Abraham A-L, Ceppi M, Conseiller E, Debuchy R, Malagnac F, Goarin A, Silar P, Lacoste S, Sallet E, Bensimon A, Giraud T, Brygoo Y. 2014. Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nat Commun 5:2876 http://dx.doi.org/10.1038/ncomms3876. [PubMed]
54. Selmecki A, Forche A, Berman J. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313:367–370 http://dx.doi.org/10.1126/science.1128242. [PubMed]
55. Ni M, Feretzaki M, Li W, Floyd-Averette A, Mieczkowski P, Dietrich FS, Heitman J. 2013. Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol 11:e1001653 http://dx.doi.org/10.1371/journal.pbio.1001653. [PubMed]
56. Farrer RA, Henk DA, Garner TWJ, Balloux F, Woodhams DC, Fisher MC. 2013. Chromosomal copy number variation, selection and uneven rates of recombination reveal cryptic genome diversity linked to pathogenicity. PLoS Genet 9:e1003703 http://dx.doi.org/10.1371/journal.pgen.1003703. [PubMed]
57. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, Eastman JM, Richards-Hrdlicka K, Joneson S, Jenkinson TS, Longcore JE, Parra Olea G, Toledo LF, Arellano ML, Medina EM, Restrepo S, Flechas SV, Berger L, Briggs CJ, Stajich JE. 2013. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci USA 110:9385–9390 http://dx.doi.org/10.1073/pnas.1300130110. [PubMed]
58. Refsnider JM, Poorten TJ, Langhammer PF, Burrowes PA, Rosenblum EB. 2015. Genomic correlates of virulence attenuation in the deadly amphibian chytrid fungus, Batrachochytrium dendrobatidis. G3 (Bethesda) 5:2291–2298 http://dx.doi.org/10.1534/g3.115.021808. [PubMed]
59. Ma L-J, Geiser DM, Proctor RH, Rooney AP, O’Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K. 2013. Fusarium pathogenomics. Annu Rev Microbiol 67:399–416 http://dx.doi.org/10.1146/annurev-micro-092412-155650. [PubMed]
60. Schardl CL, Leuchtmann A, Spiering MJ. 2004. Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340 http://dx.doi.org/10.1146/annurev.arplant.55.031903.141735. [PubMed]
61. Bennett RJ, Forche A, Berman J. 2014. Rapid mechanisms for generating genome diversity: whole ploidy shifts, aneuploidy, and loss of heterozygosity. Cold Spring Harb Perspect Med 4:a019604 http://dx.doi.org/10.1101/cshperspect.a019604. [PubMed]
62. Dunkel N, Blass J, Rogers PD, Morschhäuser J. 2008. Mutations in the multi-drug resistance regulator MRR1, followed by loss of heterozygosity, are the main cause of MDR1 overexpression in fluconazole-resistant Candida albicans strains. Mol Microbiol 69:827–840 http://dx.doi.org/10.1111/j.1365-2958.2008.06309.x. [PubMed]
63. Gerstein AC, Kuzmin A, Otto SP. 2014. Loss-of-heterozygosity facilitates passage through Haldane’s sieve for Saccharomyces cerevisiae undergoing adaptation. Nat Commun 5:3819 http://dx.doi.org/10.1038/ncomms4819. [PubMed]
64. James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW, Fisher MC, Berger L, Weldon C, du Preez L, Longcore JE. 2009. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog 5:e1000458 http://dx.doi.org/10.1371/journal.ppat.1000458. [PubMed]
65. Vakirlis N, Sarilar V, Drillon G, Fleiss A, Agier N, Meyniel JP, Blanpain L, Carbone A, Devillers H, Dubois K, Gillet-Markowska A, Graziani S, Huu-Vang N, Poirel M, Reisser C, Schott J, Schacherer J, Lafontaine I, Llorente B, Neuvéglise C, Fischer G. 2016. Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus. Genome Res 26:918–932 http://dx.doi.org/10.1101/gr.204420.116. [PubMed]
66. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GHJ, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJGM, Zhong S, Goodwin SB, Grigoriev IV. 2012. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8:e1003037 http://dx.doi.org/10.1371/journal.ppat.1003037. (Erratum, 9(3) :10.1371/annotation/fcca88ac-d684-46e0-a483-62af67e777bd.)
67. Hane JK, Rouxel T, Howlett BJ, Kema GHJ, Goodwin SB, Oliver RP. 2011. A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol 12:R45 http://dx.doi.org/10.1186/gb-2011-12-5-r45. [PubMed]
68. Ellison CE, Stajich JE, Jacobson DJ, Natvig DO, Lapidus A, Foster B, Aerts A, Riley R, Lindquist EA, Grigoriev IV, Taylor JW. 2011. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189:55–69 http://dx.doi.org/10.1534/genetics.111.130690. [PubMed]
69. Whittle CA, Johannesson H. 2011. Evidence of the accumulation of allele-specific non-synonymous substitutions in the young region of recombination suppression within the mating-type chromosomes of Neurospora tetrasperma. Hered Edinb 107:305–314 http://dx.doi.org/10.1038/hdy.2011.11. [PubMed]
70. Lengeler KB, Fox DS, Fraser JA, Allen A, Forrester K, Dietrich FS, Heitman J. 2002. Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell 1:704–718 http://dx.doi.org/10.1128/EC.1.5.704-718.2002. [PubMed]
71. Fraser JA, Hsueh YP, Findley KM, Heitman J. 2007. Evolution of the mating-type locus: the Basidiomycetes, p 19–34. In Heitman J, Kronstad J, Taylor J, Casselton L (ed), Sex in Fungi: Molecular Determination and Evolutionary Implications. ASM Press, Washington, DC. 10.1037/11499-002.
72. Giraud T, Yockteng R, López-Villavicencio M, Refrégier G, Hood ME. 2008. Mating system of the anther smut fungus Microbotryum violaceum: selfing under heterothallism. Eukaryot Cell 7:765–775 http://dx.doi.org/10.1128/EC.00440-07. [PubMed]
73. Votintseva AA, Filatov DA. 2009. Evolutionary strata in a small mating-type-specific region of the smut fungus Microbotryum violaceum. Genetics 182:1391–1396 http://dx.doi.org/10.1534/genetics.109.103192. [PubMed]
74. Branco S, Badouin H, Rodríguez de la Vega RC, Gouzy J, Carpentier F, Aguileta G, Siguenza S, Brandenburg J-T, Coelho MA, Hood ME, Giraud T. Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism. Proc Natl Acad Sci USA 114:7067–7072. [PubMed]
75. 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 23:1271–1282 http://dx.doi.org/10.1101/gr.152660.112. [PubMed]
76. Barton N. 2010. Understanding adaptation in large populations. PLoS Genet 6:e1000987 http://dx.doi.org/10.1371/journal.pgen.1000987. [PubMed]
77. Baranova MA, Logacheva MD, Penin AA, Seplyarskiy VB, Safonova YY, Naumenko SA, Klepikova AV, Gerasimov ES, Bazykin GA, James TY, Kondrashov AS. 2015. Extraordinary genetic diversity in a wood decay mushroom. Mol Biol Evol 32:2775–2783 http://dx.doi.org/10.1093/molbev/msv153. [PubMed]
78. Cutter AD, Jovelin R, Dey A. 2013. Molecular hyperdiversity and evolution in very large populations. Mol Ecol 22:2074–2095 http://dx.doi.org/10.1111/mec.12281. [PubMed]
79. Taylor JW, Hann-Soden C, Branco S, Sylvain I, Ellison CE. 2015. Clonal reproduction in fungi. Proc Natl Acad Sci USA 112:8901–8908 http://dx.doi.org/10.1073/pnas.1503159112. [PubMed]
80. Goddard MR, Godfray HCJ, Burt A. 2005. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434:636–640 http://dx.doi.org/10.1038/nature03405. [PubMed]
81. Voss H-H, Bowden RL, Leslie JF, Miedaner T. 2010. Variation and transgression of aggressiveness among two Gibberella zeae crosses developed from highly aggressive parental isolates. Phytopathology 100:904–912 http://dx.doi.org/10.1094/PHYTO-100-9-0904. [PubMed]
82. Brasier CM. 1987. The dynamics of fungal speciation, p 231–260. In Rayner ADM, Brasier CM, Moore D (ed), Evolutionary Biology of the Fungi. Cambridge University Press, Cambridge, United Kingdom.
83. Friedman N, Rando OJ. 2015. Epigenomics and the structure of the living genome. Genome Res 25:1482–1490 http://dx.doi.org/10.1101/gr.190165.115. [PubMed]
84. Flusberg BA, Webster DR, Lee JH, Travers KJ, Olivares EC, Clark TA, Korlach J, Turner SW. 2010. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 7:461–465 http://dx.doi.org/10.1038/nmeth.1459. [PubMed]
85. Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P. 1996. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010. [PubMed]
86. Bonfante P, Anca IA. 2009. Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383 http://dx.doi.org/10.1146/annurev.micro.091208.073504. [PubMed]
87. Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P. 2016. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10:130–144 http://dx.doi.org/10.1038/ismej.2015.91. [PubMed]
88. Mondo SJ, Salvioli A, Bonfante P, Morton JB, Pawlowska TE. 2016. Nondegenerative evolution in ancient heritable bacterial endosymbionts of fungi. Mol Biol Evol 33:2216–2231 http://dx.doi.org/10.1093/molbev/msw086. [PubMed]
89. Naito M, Pawlowska TE. 2016. Defying Muller’s ratchet: ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity. MBio 7:e02057-15 http://dx.doi.org/10.1128/mBio.02057-15. [PubMed]
90. Partida-Martinez LP, Hertweck C. 2007. A gene cluster encoding rhizoxin biosynthesis in “ Burkholderia rhizoxina”, the bacterial endosymbiont of the fungus Rhizopus microsporus. ChemBioChem 8:41–45 http://dx.doi.org/10.1002/cbic.200600393. [PubMed]
91. Choi GH, Nuss DL. 1992. Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800–803 http://dx.doi.org/10.1126/science.1496400. [PubMed]
92. Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ. 2007. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515 http://dx.doi.org/10.1126/science.1136237. [PubMed]
93. Nuss DL. 2011. Mycoviruses, RNA silencing, and viral RNA recombination. Adv Virus Res 80:25–48 http://dx.doi.org/10.1016/B978-0-12-385987-7.00002-6. [PubMed]
94. Marzano SYL, Nelson BD, Ajayi-Oyetunde O, Bradley CA, Hughes TJ, Hartman GL, Eastburn DM, Domier LL. 2016. Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J Virol 90:6846–6863 http://dx.doi.org/10.1128/JVI.00357-16. [PubMed]
95. Edwards MD, Symbor-Nagrabska A, Dollard L, Gifford DK, Fink GR. 2014. Interactions between chromosomal and nonchromosomal elements reveal missing heritability. Proc Natl Acad Sci USA 111:7719–7722 http://dx.doi.org/10.1073/pnas.1407126111. [PubMed]
96. May G, Taylor JW. 1988. Patterns of mating and mitochondrial DNA inheritance in the agaric Basidiomycete Coprinus cinereus. Genetics 118:213–220. [PubMed]
97. Lee SB, Taylor JW. 1993. Uniparental inheritance and replacement of mitochondrial DNA in Neurospora tetrasperma. Genetics 134:1063–1075. [PubMed]
98. Turner E, Jacobson DJ, Taylor JW. 2011. Genetic architecture of a reinforced, postmating, reproductive isolation barrier between Neurospora species indicates evolution via natural selection. PLoS Genet 7:e1002204 http://dx.doi.org/10.1371/journal.pgen.1002204. [PubMed]
99. Cubillos FA, Parts L, Salinas F, Bergström A, Scovacricchi E, Zia A, Illingworth CJR, Mustonen V, Ibstedt S, Warringer J, Louis EJ, Durbin R, Liti G. 2013. High-resolution mapping of complex traits with a four-parent advanced intercross yeast population. Genetics 195:1141–1155 http://dx.doi.org/10.1534/genetics.113.155515. [PubMed]
100. Wenger JW, Schwartz K, Sherlock G. 2010. Bulk segregant analysis by high-throughput sequencing reveals a novel xylose utilization gene from Saccharomyces cerevisiae. PLoS Genet 6:e1000942 http://dx.doi.org/10.1371/journal.pgen.1000942. [PubMed]
101. Sigwalt A, Caradec C, Brion C, Hou J, de Montigny J, Jung P, Fischer G, Llorente B, Friedrich A, Schacherer J. 2016. Dissection of quantitative traits by bulk segregant mapping in a protoploid yeast species. FEMS Yeast Res 16:fow056 http://dx.doi.org/10.1093/femsyr/fow056. [PubMed]
102. Pomraning KR, Smith KM, Freitag M. 2011. Bulk segregant analysis followed by high-throughput sequencing reveals the Neurospora cell cycle gene, ndc-1, to be allelic with the gene for ornithine decarboxylase, spe-1. Eukaryot Cell 10:724–733 http://dx.doi.org/10.1128/EC.00016-11. [PubMed]
103. Heller J, Zhao J, Rosenfield G, Kowbel DJ, Gladieux P, Glass NL. 2016. Characterization of greenbeard genes involved in long-distance kind discrimination in a microbial eukaryote. PLoS Biol 14:e1002431 http://dx.doi.org/10.1371/journal.pbio.1002431. [PubMed]
104. Li YF, Costello JC, Holloway AK, Hahn MW. 2008. “Reverse ecology” and the power of population genomics. Evolution 62:2984–2994 http://dx.doi.org/10.1111/j.1558-5646.2008.00486.x. [PubMed]
105. Palma-Guerrero J, Hall CR, Kowbel D, Welch J, Taylor JW, Brem RB, Glass NL. 2013. Genome wide association identifies novel loci involved in fungal communication. PLoS Genet 9:e1003669 http://dx.doi.org/10.1371/journal.pgen.1003669. [PubMed]
106. Dalman K, Himmelstrand K, Olson Å, Lind M, Brandström-Durling M, Stenlid J. 2013. A genome-wide association study identifies genomic regions for virulence in the non-model organism Heterobasidion annosum s.s. PLoS One 8:e53525 http://dx.doi.org/10.1371/journal.pone.0053525. [PubMed]
107. Plissonneau C, Benevenuto J, Mohd-Assaad N, Fouché S, Hartmann FE, Croll D. 2017. Using population and comparative genomics to understand the genetic basis of effector-driven fungal pathogen evolution. Front Plant Sci 8:119 http://dx.doi.org/10.3389/fpls.2017.00119. [PubMed]
108. Gao Y, Liu Z, Faris JD, Richards J, Brueggeman RS, Li X, Oliver RP, McDonald BA, Friesen TL. 2016. Validation of genome-wide association studies as a tool to identify virulence factors in Parastagonospora nodorum. Phytopathology 106:1177–1185 http://dx.doi.org/10.1094/PHYTO-02-16-0113-FI. [PubMed]
109. Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C, Zala M, Ducasse A, Confais J, Compain J, Lapalu N, Amselem J, McDonald BA, Croll D, Palma-Guerrero J. 2017. A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol 214:619–631 http://dx.doi.org/10.1111/nph.14434. [PubMed]
110. 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 29:417–430 http://dx.doi.org/10.1094/MPMI-09-15-0218-R. [PubMed]
111. 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. Proc Natl Acad Sci USA 109:10954–10959 http://dx.doi.org/10.1073/pnas.1201403109. [PubMed]
112. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL, Taylor JW. 2011. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci USA 108:2831–2836 http://dx.doi.org/10.1073/pnas.1014971108. [PubMed]
113. Cruickshank TE, Hahn MW. 2014. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23:3133–3157 http://dx.doi.org/10.1111/mec.12796. [PubMed]
114. Noor MAF, Bennett SM. 2009. Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Hered Edinb 103:439–444 http://dx.doi.org/10.1038/hdy.2009.151. [PubMed]
115. Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJT, van Oudenaarden A, Barton DBH, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ. 2009. Population genomics of domestic and wild yeasts. Nature 458:337–341 http://dx.doi.org/10.1038/nature07743. [PubMed]
116. Wang QM, Liu WQ, Liti G, Wang SA, Bai FY. 2012. Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity. Mol Ecol 21:5404–5417 http://dx.doi.org/10.1111/j.1365-294X.2012.05732.x. [PubMed]
117. Peter J, Schacherer J. 2016. Population genomics of yeasts: towards a comprehensive view across a broad evolutionary scale. Yeast 33:73–81 http://dx.doi.org/10.1002/yea.3142. [PubMed]
118. Roop JI, Chang KC, Brem RB. 2016. Polygenic evolution of a sugar specialization trade-off in yeast. Nature 530:336–339 http://dx.doi.org/10.1038/nature16938. [PubMed]
119. Koufopanou V, Hughes J, Bell G, Burt A. 2006. The spatial scale of genetic differentiation in a model organism: the wild yeast Saccharomyces paradoxus. Philos Trans R Soc Lond B Biol Sci 361:1941–1946 http://dx.doi.org/10.1098/rstb.2006.1922. [PubMed]
120. Leducq J-B, Charron G, Samani P, Dubé AK, Sylvester K, James B, Almeida P, Sampaio JP, Hittinger CT, Bell G, Landry CR. 2014. Local climatic adaptation in a widespread microorganism. Proc Biol Sci 281:20132472 http://dx.doi.org/10.1098/rspb.2013.2472. [PubMed]
121. Leducq JB. 2014. Ecological genomics of adaptation and speciation in fungi. Adv Exp Med Biol 781:49–72 http://dx.doi.org/10.1007/978-94-007-7347-9_4. [PubMed]
122. Leducq JB, Nielly-Thibault L, Charron G, Eberlein C, Verta JP, Samani P, Sylvester K, Hittinger CT, Bell G, Landry CR. 2016. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat Microbiol 1:15003. doi:10.1038/nmicrobiol.2015.3. [PubMed]
123. Turner BC, Perkins DD, Fairfield A. 2001. Neurospora from natural populations: a global study. Fungal Genet Biol 32:67–92 http://dx.doi.org/10.1006/fgbi.2001.1247. [PubMed]
124. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103:10352–10357 http://dx.doi.org/10.1073/pnas.0601456103. [PubMed]
125. Dettman JR, Jacobson DJ, Taylor JW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720 http://dx.doi.org/10.1111/j.0014-3820.2003.tb01514.x. [PubMed]
126. Nachman MW, Hoekstra HE, D’Agostino SL. 2003. The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100:5268–5273 http://dx.doi.org/10.1073/pnas.0431157100. [PubMed]
127. Branco S, Gladieux P, Ellison CE, Kuo A, LaButti K, Lipzen A, Grigoriev IV, Liao HL, Vilgalys R, Peay KG, Taylor JW, Bruns TD. 2015. Genetic isolation between two recently diverged populations of a symbiotic fungus. Mol Ecol 24:2747–2758 http://dx.doi.org/10.1111/mec.13132. [PubMed]
128. Tang H, Peng J, Wang P, Risch NJ. 2005. Estimation of individual admixture: analytical and study design considerations. Genet Epidemiol 28:289–301 http://dx.doi.org/10.1002/gepi.20064. [PubMed]
129. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5:e1000695 http://dx.doi.org/10.1371/journal.pgen.1000695. [PubMed]
130. Branco S, Bi K, Liao H-L, Gladieux P, Badouin H, Ellison CE, Nguyen NH, Vilgalys R, Peay KG, Taylor JW, Bruns TD. 2017. Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes. Mol Ecol 26:2063–2076 http://dx.doi.org/10.1111/mec.13892. [PubMed]
131. Neafsey DE, Barker BM, Sharpton TJ, Stajich JE, Park DJ, Whiston E, Hung CY, McMahan C, White J, Sykes S, Heiman D, Young S, Zeng Q, Abouelleil A, Aftuck L, Bessette D, Brown A, FitzGerald M, Lui A, Macdonald JP, Priest M, Orbach MJ, Galgiani JN, Kirkland TN, Cole GT, Birren BW, Henn MR, Taylor JW, Rounsley SD. 2010. Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control. Genome Res 20:938–946 http://dx.doi.org/10.1101/gr.103911.109. [PubMed]
132. Fisher MC, Koenig GL, White TJ, San-Blas G, Negroni R, Alvarez IG, Wanke B, Taylor JW. 2001. Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proc Natl Acad Sci USA 98:4558–4562 http://dx.doi.org/10.1073/pnas.071406098. [PubMed]
133. Fisher MC, Koenig GL, White TJ, Taylor JW. 2002. Molecular and phenotypic description of Coccidioides posadasii sp. nov., previously recognized as the non-California population of Coccidioides immitis. Mycologia 94:73–84 http://dx.doi.org/10.1080/15572536.2003.11833250. [PubMed]
134. Hung CY, Seshan KR, Yu JJ, Schaller R, Xue J, Basrur V, Gardner MJ, Cole GT. 2005. A metalloproteinase of Coccidioides posadasii contributes to evasion of host detection. Infect Immun 73:6689–6703 http://dx.doi.org/10.1128/IAI.73.10.6689-6703.2005. [PubMed]
135. Whiston E, Zhang Wise H, Sharpton TJ, Jui G, Cole GT, Taylor JW. 2012. Comparative transcriptomics of the saprobic and parasitic growth phases in Coccidioides spp. PLoS One 7:e41034 http://dx.doi.org/10.1371/journal.pone.0041034. [PubMed]
136. Billmyre RB, Croll D, Li W, Mieczkowski P, Carter DA, Cuomo CA, Kronstad JW, Heitman J. 2014. Highly recombinant VGII Cryptococcus gattii population develops clonal outbreak clusters through both sexual macroevolution and asexual microevolution. MBio 5:e01494-14 http://dx.doi.org/10.1128/mBio.01494-14. [PubMed]
137. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, Falk R, Parnmen S, Lumbsch HT, Boekhout T. 2015. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol 78:16–48 http://dx.doi.org/10.1016/j.fgb.2015.02.009. [PubMed]
138. Engelthaler DM, Hicks ND, Gillece JD, Roe CC, Schupp JM, Driebe EM, Gilgado F, Carriconde F, Trilles L, Firacative C, Ngamskulrungroj P, Castañeda E, Lazera MS, Melhem MSC, Pérez-Bercoff A, Huttley G, Sorrell TC, Voelz K, May RC, Fisher MC, Thompson GR III, Lockhart SR, Keim P, Meyer W. 2014. Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. MBio 5:e01464-14 http://dx.doi.org/10.1128/mBio.01464-14. [PubMed]
139. Hagen F, Ceresini PC, Polacheck I, Ma H, van Nieuwerburgh F, Gabaldón T, Kagan S, Pursall ER, Hoogveld HL, van Iersel LJJ, Klau GW, Kelk SM, Stougie L, Bartlett KH, Voelz K, Pryszcz LP, Castañeda E, Lazera M, Meyer W, Deforce D, Meis JF, May RC, Klaassen CHW, Boekhout T. 2013. Ancient dispersal of the human fungal pathogen Cryptococcus gattii from the Amazon rainforest. PLoS One 8:e71148 http://dx.doi.org/10.1371/journal.pone.0071148. [PubMed]
140. Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S, Schaefer LK, Shimizu KK, Valenti L, Zbinden H, Wicker T, Keller B. 2016. Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat Genet 48:201–205 http://dx.doi.org/10.1038/ng.3485. [PubMed]
141. Gladieux P, Wilson BA, Perraudeau F, Montoya LA, Kowbel D, Hann-Soden C, Fischer M, Sylvain I, Jacobson DJ, Taylor JW. 2015. Genomic sequencing reveals historical, demographic and selective factors associated with the diversification of the fire-associated fungus Neurospora discreta. Mol Ecol 24:5657–5675 http://dx.doi.org/10.1111/mec.13417. [PubMed]
142. Chomvong K, Lin E, Blaisse M, Gillespie AE, Cate JHD. 2017. Relief of xylose binding to cellobiose phosphorylase by a single distal mutation. ACS Synth Biol 6:206–210 http://dx.doi.org/10.1021/acssynbio.6b00211. [PubMed]
143. Nødvig CS, Nielsen JB, Kogle ME, Mortensen UH. 2015. A CRISPR-Cas9 system for genetic engineering of filamentous fungi. PLoS One 10:e0133085 http://dx.doi.org/10.1371/journal.pone.0133085. [PubMed]
144. Liu R, Chen L, Jiang Y, Zhou Z, Zou G. 2015. Efficient genome editing in filamentous fungus Trichoderma reesei using the CRISPR/Cas9 system. Cell Discov 1:15007 http://dx.doi.org/10.1038/celldisc.2015.7. [PubMed]
145. Arazoe T, Miyoshi K, Yamato T, Ogawa T, Ohsato S, Arie T, Kuwata S. 2015. Tailor-made CRISPR/Cas system for highly efficient targeted gene replacement in the rice blast fungus. Biotechnol Bioeng 112:2543–2549 http://dx.doi.org/10.1002/bit.25662. [PubMed]
146. Schuster M, Schweizer G, Reissmann S, Kahmann R. 2016. Genome editing in Ustilago maydis using the CRISPR-Cas system. Fungal Genet Biol 89:3–9 http://dx.doi.org/10.1016/j.fgb.2015.09.001. [PubMed]
147. Mitchell AP. 2017. Location, location, location: use of CRISPR-Cas9 for genome editing in human pathogenic fungi. PLoS Pathog 13:e1006209 http://dx.doi.org/10.1371/journal.ppat.1006209. [PubMed]
148. Ma L-J, et al. 2010. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464:367–373 http://dx.doi.org/10.1038/nature08850. [PubMed]
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2017-09-22
2020-09-19

Abstract:

The first eukaryotic genome to be sequenced was fungal, and there continue to be more sequenced genomes in the kingdom Fungi than in any other eukaryotic kingdom. Comparison of these genomes reveals many sources of genetic variation, from single nucleotide polymorphisms to horizontal gene transfer and on to changes in the arrangement and number of chromosomes, not to mention endofungal bacteria and viruses. Population genomics shows that all sources generate variation all the time and implicate natural selection as the force maintaining genome stability. Variation in wild populations is a rich resource for associating genetic variation with phenotypic variation, whether through quantitative trait locus mapping, genome-wide association studies, or reverse ecology. Subjects of studies associating genetic and phenotypic variation include model fungi, e.g., and , but pioneering studies have also been made with fungi pathogenic to plants, e.g., (= ), , and , and to humans, e.g., , , and .

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Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity
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Citation: Taylor J, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, Gladieux P. 2017. Sources of fungal genetic variation and associating it with phenotypic diversity. microbiolspec 5(5): doi:10.1128/microbiolspec.FUNK-0057-2016
/content/microbiolspec/10.1128/microbiolspec.FUNK-0057-2016.fig1
FIGURE 1
Gene family Bayesian phylogeny for proteinase genes with S8 domains showing (top) some phylogenetic lineages with no expansion and (below) others with a large expansion due to nine gene duplications (asterisks). Key to taxon abbreviations preceding gene identifiers: (aory), (afum), (anid), (uree), (cimm), (cpos), (sscl), (bcin), (snod), (mgri), (tree), (lbic), and (ccin). Adapted from reference 24 .
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FIGURE 1

Gene family Bayesian phylogeny for proteinase genes with S8 domains showing (top) some phylogenetic lineages with no expansion and (below) others with a large expansion due to nine gene duplications (asterisks). Key to taxon abbreviations preceding gene identifiers: (aory), (afum), (anid), (uree), (cimm), (cpos), (sscl), (bcin), (snod), (mgri), (tree), (lbic), and (ccin). Adapted from reference 24 .

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FIGURE 2
Diagrams showing aneuploidy and loss of heterozygosity (LOH) in haploid and diploid genomes. Each individual has seven distinct chromosomes colored to show heterozygosity.
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FIGURE 2

Diagrams showing aneuploidy and loss of heterozygosity (LOH) in haploid and diploid genomes. Each individual has seven distinct chromosomes colored to show heterozygosity.

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FIGURE 3
Contour-clamped homogeneous electric field gel karyotype of chromosomes showing conditionally dispensable chromosomes (CDCs) and their transmission between strains. Donor strain 007 (left) harbors CDCs 1 and 2 (arrows), and recipient strain -47 (right) lacks them. Strains 1A-3C (middle lanes) are derived from simple coincubation of 007 and -47. These strains have the -47 karyotype and have gained CDCs 1 or 2 (arrows), or both, from 007. Southern hybridization of the contour-clamped homogeneous electric field gel to a probe with DNA from CDC 1 (), confirming the presence of CDC 1 in donor strain 007 and progeny strains 1A-3C, which possess the karyotype of the recipient strain -47. Adapted from reference 148 .
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FIGURE 3

Contour-clamped homogeneous electric field gel karyotype of chromosomes showing conditionally dispensable chromosomes (CDCs) and their transmission between strains. Donor strain 007 (left) harbors CDCs 1 and 2 (arrows), and recipient strain -47 (right) lacks them. Strains 1A-3C (middle lanes) are derived from simple coincubation of 007 and -47. These strains have the -47 karyotype and have gained CDCs 1 or 2 (arrows), or both, from 007. Southern hybridization of the contour-clamped homogeneous electric field gel to a probe with DNA from CDC 1 (), confirming the presence of CDC 1 in donor strain 007 and progeny strains 1A-3C, which possess the karyotype of the recipient strain -47. Adapted from reference 148 .

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FIGURE 4
Population structure. Bayesian phylogenetic analysis of SNPs from transcriptomes of 50 individuals from around the Gulf of Mexico showing that individuals thought to form one population actually are found in seven populations. Adapted from reference 112 . Bayesian phylogenetic analysis of SNPs from transcriptomes of 112 individuals from the same geographic area as the Louisiana population in A showing no population subdivision. Note the many individuals with the same genotype as the laboratory strain, FGSC 2489, indicative of mistakes made in transferring isolates. Adapted from reference 103 .
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FIGURE 4

Population structure. Bayesian phylogenetic analysis of SNPs from transcriptomes of 50 individuals from around the Gulf of Mexico showing that individuals thought to form one population actually are found in seven populations. Adapted from reference 112 . Bayesian phylogenetic analysis of SNPs from transcriptomes of 112 individuals from the same geographic area as the Louisiana population in A showing no population subdivision. Note the many individuals with the same genotype as the laboratory strain, FGSC 2489, indicative of mistakes made in transferring isolates. Adapted from reference 103 .

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FIGURE 5
Hybridization and introgression in weakly diverged populations. Hybridization and introgression can be detected in genome scans of closely related populations when the genes are introduced from a more diverged population. () Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have low divergence (yellow dots and one red dot), but one gene shows exceptionally large divergence (blue dot). () Population tree with one gene tree highlighted in yellow showing that well-diverged genes entering from older, more diverged populations (blue dots and arrows) will be detected by comparison with the low divergence in the rest of the genome. However, genes exchanged between the populations will be missed (red dots and arrows) due to their low divergence being indistinguishable from the rest of the genome.
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FIGURE 5

Hybridization and introgression in weakly diverged populations. Hybridization and introgression can be detected in genome scans of closely related populations when the genes are introduced from a more diverged population. () Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have low divergence (yellow dots and one red dot), but one gene shows exceptionally large divergence (blue dot). () Population tree with one gene tree highlighted in yellow showing that well-diverged genes entering from older, more diverged populations (blue dots and arrows) will be detected by comparison with the low divergence in the rest of the genome. However, genes exchanged between the populations will be missed (red dots and arrows) due to their low divergence being indistinguishable from the rest of the genome.

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FIGURE 6
Hybridization and introgression in strongly diverged populations or species. Hybridization and introgression can be detected in genome scans of distantly related populations or species when the gene flow is between the two well-diverged groups. () Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have high divergence (yellow dots and one red dot), but one gene shows exceptionally low divergence (blue dot). () Population tree with one gene tree highlighted in yellow showing that genes exchanged between the populations will be detected (blue dots and arrows) due to their lack of divergence compared to the high divergence of the rest of the genome. However, genes entering from populations from other well-diverged lineages (red dots and arrows) will show divergence similar to the rest of the genome and be missed.
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FIGURE 6

Hybridization and introgression in strongly diverged populations or species. Hybridization and introgression can be detected in genome scans of distantly related populations or species when the gene flow is between the two well-diverged groups. () Genome scan by Fst (a measure of relative genetic divergence) showing that nearly all genes have high divergence (yellow dots and one red dot), but one gene shows exceptionally low divergence (blue dot). () Population tree with one gene tree highlighted in yellow showing that genes exchanged between the populations will be detected (blue dots and arrows) due to their lack of divergence compared to the high divergence of the rest of the genome. However, genes entering from populations from other well-diverged lineages (red dots and arrows) will show divergence similar to the rest of the genome and be missed.

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0057-2016
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FIGURE 7
Regions of extreme divergence between populations of . Rows are aligned genomes of Louisiana (LA), Caribbean (Carib), and other populations (out) seen in Fig. 4 . Columns are nucleotide positions in four colors for the four bases. Highlighted is the region of high divergence between the Louisiana population and the Caribbean and other populations. The genome variation in this region is consistent with a history in the Louisiana population of hybridization and introgression. Low variation among Louisiana individuals in this region is consistent with a recent selective sweep. Variation in the length of introgressed regions in the Louisiana population may indicate that the sweep is still in progress. Among the six genes in the region of divergence is -like, which codes for a prefoldin that chaperones cold-sensitive proteins. Adapted from reference 112 .
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FIGURE 7

Regions of extreme divergence between populations of . Rows are aligned genomes of Louisiana (LA), Caribbean (Carib), and other populations (out) seen in Fig. 4 . Columns are nucleotide positions in four colors for the four bases. Highlighted is the region of high divergence between the Louisiana population and the Caribbean and other populations. The genome variation in this region is consistent with a history in the Louisiana population of hybridization and introgression. Low variation among Louisiana individuals in this region is consistent with a recent selective sweep. Variation in the length of introgressed regions in the Louisiana population may indicate that the sweep is still in progress. Among the six genes in the region of divergence is -like, which codes for a prefoldin that chaperones cold-sensitive proteins. Adapted from reference 112 .

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FIGURE 8
Evidence of recent hybridization. Genome scans for introgressed DNA in the 20 largest contigs of eight individuals from the Alaska-European lineage. Numbers of SNPs introgressed from the New Mexico-Washington (NM-WA) lineage are shown on the axis. Alaskan strain AKFA12 stands out as having 12% of its genome introgressed from the NM-WA lineage, as expected from a few matings between a hybrid individual and members of the Alaskan population. Adapted from reference 141 .
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FIGURE 8

Evidence of recent hybridization. Genome scans for introgressed DNA in the 20 largest contigs of eight individuals from the Alaska-European lineage. Numbers of SNPs introgressed from the New Mexico-Washington (NM-WA) lineage are shown on the axis. Alaskan strain AKFA12 stands out as having 12% of its genome introgressed from the NM-WA lineage, as expected from a few matings between a hybrid individual and members of the Alaskan population. Adapted from reference 141 .

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Tables

Sources of Fungal Genetic Variation and Associating It with Phenotypic Diversity
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Citation: Taylor J, Branco S, Gao C, Hann-Soden C, Montoya L, Sylvain I, Gladieux P. 2017. Sources of fungal genetic variation and associating it with phenotypic diversity. microbiolspec 5(5): doi:10.1128/microbiolspec.FUNK-0057-2016
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TABLE 1
Genetic variation and its use in associating genotype and phenotype
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TABLE 1

Genetic variation and its use in associating genotype and phenotype

Source: microbiolspec September 2017 vol. 5 no. 5 doi:10.1128/microbiolspec.FUNK-0057-2016

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