Advertisement

pp 1-24 | Cite as

Yeast Population Genomics Goes Wild: The Case of Saccharomyces paradoxus

  • Mathieu Hénault
  • Chris Eberlein
  • Guillaume Charron
  • Éléonore Durand
  • Lou Nielly-Thibault
  • Hélène Martin
  • Christian R. Landry
Chapter
Part of the Population Genomics book series

Abstract

Speciation and adaptation are important processes that are difficult to study in the invisible microbial world because of the lack of easily identifiable characters that can be correlated with species boundaries and adaptive traits. Genomic tools can be used to assess and measure the genetic and genomic bases of species and population differentiation. This allows for the identification of the genes that are potential targets of natural selection and thus that underlie adaptation to specific environments. Here, we illustrate how useful this approach is by describing recent progress on microbial genomics empowered by studying Saccharomyces paradoxus in the wild. These studies have revealed the spatial and temporal scales at which fungal populations diverge, a quantification of the life history parameters of this yeast and its mechanisms of speciation, which include allopatric speciation driven by geographical barriers and hybrid speciation driven by chromosomal reorganization. Altogether, these studies establish S. paradoxus as an extremely powerful model in microbial population genomics.

Keywords

Adaptation Hybridization Introgression Population genomics Saccharomyces paradoxus Speciation Yeast 

Notes

Acknowledgments

The authors thank Anna Fijarczyk and Souhir Marsit for comments on the manuscript. This work was supported by a NSERC Discovery Grant to CRL. CRL holds the Canada Research Chair in Evolutionary Cell and Systems Biology.

References

  1. Almeida P, Barbosa R, Bensasson D, Goncalves P, Sampaio JP. Adaptive divergence in wine yeasts and their wild relatives suggests a prominent role for introgressions and rapid evolution at noncoding sites. Mol Ecol. 2017;26(7):2167–82.  https://doi.org/10.1111/mec.14071.CrossRefPubMedGoogle Scholar
  2. April J, Hanner RH, Dion-Cote AM, Bernatchez L. Glacial cycles as an allopatric speciation pump in north-eastern American freshwater fishes. Mol Ecol. 2013;22(2):409–22.  https://doi.org/10.1111/mec.12116.CrossRefPubMedGoogle Scholar
  3. Barbosa R, Almeida P, Safar SV, Santos RO, Morais PB, Nielly-Thibault L, Leducq JB, Landry CR, Goncalves P, Rosa CA, Sampaio JP. Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae. Genome Biol Evol. 2016;8(2):317–29.  https://doi.org/10.1093/gbe/evv263.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bernardes J, Stelkens RB, Greig D. Heterosis in hybrids within and between yeast species. J Evol Biol. 2016;30(3):538–48.  https://doi.org/10.1111/jeb.13023.CrossRefGoogle Scholar
  5. Birky CW Jr. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet. 2001;35:125–48.  https://doi.org/10.1146/annurev.genet.35.102401.090231.CrossRefPubMedGoogle Scholar
  6. Boynton PJ, Stelkens R, Kowallik V, Greig D. Measuring microbial fitness in a field reciprocal transplant experiment. Mol Ecol Resour. 2017;17(3):370–80.  https://doi.org/10.1111/1755-0998.12562.CrossRefPubMedGoogle Scholar
  7. Breton S, Stewart DT. Atypical mitochondrial inheritance patterns in eukaryotes. Genome. 2015;58(10):423–31.  https://doi.org/10.1139/gen-2015-0090.CrossRefPubMedGoogle Scholar
  8. Charron G, Landry CR. No evidence for extrinsic post-zygotic isolation in a wild Saccharomyces yeast system. Biol Lett. 2017;13(6):20170197.  https://doi.org/10.1098/rsbl.2017.0197.CrossRefPubMedGoogle Scholar
  9. Charron G, Leducq JB, Bertin C, Dube AK, Landry CR. Exploring the northern limit of the distribution of Saccharomyces cerevisiae and Saccharomyces paradoxus in North America. FEMS Yeast Res. 2014a;14(2):281–8.  https://doi.org/10.1111/1567-1364.12100.CrossRefPubMedGoogle Scholar
  10. Charron G, Leducq JB, Landry CR. Chromosomal variation segregates within incipient species and correlates with reproductive isolation. Mol Ecol. 2014b;23(17):4362–72.  https://doi.org/10.1111/mec.12864.CrossRefPubMedGoogle Scholar
  11. Cheeseman K, Ropars J, Renault P, Dupont J, Gouzy J, Branca A, Abraham AL, Ceppi M, Conseiller E, Debuchy R, Malagnac F, Goarin A, Silar P, Lacoste S, Sallet E, Bensimon A, Giraud T, Brygoo Y. Multiple recent horizontal transfers of a large genomic region in cheese making fungi. Nat Commun. 2014;5:2876.  https://doi.org/10.1038/ncomms3876.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chen SJ, YH W, Huang HY, Wang CC. Saccharomyces cerevisiae possesses a stress-inducible glycyl-tRNA synthetase gene. PLoS One. 2012;7(3):e33363.  https://doi.org/10.1371/journal.pone.0033363.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  13. Chiapello H, Mallet L, Guerin C, Aguileta G, Amselem J, Kroj T, Ortega-Abboud E, Lebrun MH, Henrissat B, Gendrault A, Rodolphe F, Tharreau D, Fournier E. Deciphering genome content and evolutionary relationships of isolates from the fungus Magnaporthe oryzae attacking different host plants. Genome Biol Evol. 2015;7(10):2896–912.  https://doi.org/10.1093/gbe/evv187.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chou JY, Leu JY. Speciation through cytonuclear incompatibility: insights from yeast and implications for higher eukaryotes. BioEssays. 2010;32(5):401–11.  https://doi.org/10.1002/bies.200900162.CrossRefPubMedGoogle Scholar
  15. Desjardins CA, Giamberardino C, Sykes SM, Yu CH, Tenor JL, Chen Y, Yang T, Jones AM, Sun S, Haverkamp MR, Heitman J, Litvintseva AP, Perfect JR, Cuomo CA. Population genomics and the evolution of virulence in the fungal pathogen Cryptococcus neoformans. Genome Res. 2017;27(7):1207–19.  https://doi.org/10.1101/gr.218727.116.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Eberlein C, Nielly-Thibault L, Maaroufi H, Dube AK, Leducq JB, Charron G, Landry CR. The rapid evolution of an ohnolog contributes to the ecological specialization of incipient yeast species. Mol Biol Evol. 2017;34(9):2173–86.  https://doi.org/10.1093/molbev/msx153.CrossRefPubMedGoogle Scholar
  17. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinf. 2009;10:48.  https://doi.org/10.1186/1471-2105-10-48.CrossRefGoogle Scholar
  18. Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL, Taylor JW. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci U S A. 2011;108(7):2831–6.  https://doi.org/10.1073/pnas.1014971108.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  19. Filteau M, Charron G, Landry CR. Identification of the fitness determinants of budding yeast on a natural substrate. ISME J. 2016;11(4):959–71.  https://doi.org/10.1038/ismej.2016.170.CrossRefPubMedGoogle Scholar
  20. Ford CB, Funt JM, Abbey D, Issi L, Guiducci C, Martinez DA, Delorey T, Li BY, White TC, Cuomo C, Rao RP, Berman J, Thompson DA, Regev A. The evolution of drug resistance in clinical isolates of Candida albicans. elife. 2015;4:e00662.  https://doi.org/10.7554/eLife.00662.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gabaldon T, Martin T, Marcet-Houben M, Durrens P, Bolotin-Fukuhara M, Lespinet O, Arnaise S, Boisnard S, Aguileta G, Atanasova R, Bouchier C, Couloux A, Creno S, Almeida Cruz J, Devillers H, Enache-Angoulvant A, Guitard J, Jaouen L, Ma L, Marck C, Neuveglise C, Pelletier E, Pinard A, Poulain J, Recoquillay J, Westhof E, Wincker P, Dujon B, Hennequin C, Fairhead C. Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics. 2013;14:623.  https://doi.org/10.1186/1471-2164-14-623.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Goncalves P, Valerio E, Correia C, de Almeida JM, Sampaio JP. Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One. 2011;6(6):e20739.  https://doi.org/10.1371/journal.pone.0020739.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  23. Greig D, Louis EJ, Borts RH, Travisano M. Hybrid speciation in experimental populations of yeast. Science. 2002;298(5599):1773–5.  https://doi.org/10.1126/science.1076374.ADSCrossRefPubMedGoogle Scholar
  24. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav. 2012;7(11):1456–66.  https://doi.org/10.4161/psb.21949.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Herbst RH, Bar-Zvi D, Reikhav S, Soifer I, Breker M, Jona G, Shimoni E, Schuldiner M, Levy AA, Barkai N. Heterosis as a consequence of regulatory incompatibility. BMC Biol. 2017;15(1):38.  https://doi.org/10.1186/s12915-017-0373-7.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hittinger CT. Saccharomyces diversity and evolution: a budding model genus. Trends Genet. 2013;29(5):309–17.  https://doi.org/10.1016/j.tig.2013.01.002.CrossRefPubMedGoogle Scholar
  27. Hyma KE, Fay JC. Mixing of vineyard and oak-tree ecotypes of Saccharomyces cerevisiae in North American vineyards. Mol Ecol. 2013;22(11):2917–30.  https://doi.org/10.1111/mec.12155.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Jhuang HY, Lee HY, Leu JY. Mitochondrial-nuclear co-evolution leads to hybrid incompatibility through pentatricopeptide repeat proteins. EMBO Rep. 2017;18(1):87–101.  10.15252/embr.201643311.CrossRefPubMedGoogle Scholar
  29. Johnson LJ, Koufopanou V, Goddard MR, Hetherington R, Schafer SM, Burt A. Population genetics of the wild yeast Saccharomyces paradoxus. Genetics. 2004;166(1):43–52.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004;428(6983):617–24.  https://doi.org/10.1038/nature02424.ADSCrossRefPubMedGoogle Scholar
  31. Koufopanou V, Hughes J, Bell G, Burt A. The spatial scale of genetic differentiation in a model organism: the wild yeast Saccharomyces paradoxus. Philos Trans R Soc Lond Ser B Biol Sci. 2006;361(1475):1941–6.  https://doi.org/10.1098/rstb.2006.1922.CrossRefGoogle Scholar
  32. Kowallik V, Greig D. A systematic forest survey showing an association of Saccharomyces paradoxus with oak leaf litter. Environ Microbiol Rep. 2016;8(5):833–41.  https://doi.org/10.1111/1758-2229.12446.CrossRefGoogle Scholar
  33. Kuehne HA, Murphy HA, Francis CA, Sniegowski PD. Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations. Curr Biol. 2007;17(5):407–11.  https://doi.org/10.1016/j.cub.2006.12.047.CrossRefPubMedGoogle Scholar
  34. Lang GI, Rice DP, Hickman MJ, Sodergren E, Weinstock GM, Botstein D, Desai MM. Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature. 2013;500(7464):571–4.  https://doi.org/10.1038/nature12344.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  35. Laureau R, Loeillet S, Salinas F, Bergstrom A, Legoix-Ne P, Liti G, Nicolas A. Extensive recombination of a yeast diploid hybrid through meiotic reversion. PLoS Genet. 2016;12(2):e1005781.  https://doi.org/10.1371/journal.pgen.1005781.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Leducq JB, Charron G, Diss G, Gagnon-Arsenault I, Dube AK, Landry CR. Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genet. 2012;8(12):e1003161.  https://doi.org/10.1371/journal.pgen.1003161.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Leducq JB, Charron G, Samani P, Dube AK, Sylvester K, James B, Almeida P, Sampaio JP, Hittinger CT, Bell G, Landry CR. Local climatic adaptation in a widespread microorganism. Proc Biol Sci. 2014;281(1777):20132472.  https://doi.org/10.1098/rspb.2013.2472.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Leducq JB, Nielly-Thibault L, Charron G, Eberlein C, Verta JP, Samani P, Sylvester K, Hittinger CT, Bell G, Landry CR. Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nat Microbiol. 2016;1:15003.  https://doi.org/10.1038/nmicrobiol.2015.3.CrossRefPubMedGoogle Scholar
  39. Leducq JB, Henault M, Charron G, Nielly-Thibault L, Terrat Y, Fiumera HL, Jesse Shapiro B, Landry CR. Mitochondrial recombination and introgression during speciation by hybridization. Mol Biol Evol. 2017;34(8):1947–59.  https://doi.org/10.1093/molbev/msx139.CrossRefPubMedGoogle Scholar
  40. 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 MJ, van Oudenaarden A, Barton DB, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ. Population genomics of domestic and wild yeasts. Nature. 2009;458(7236):337–41.  https://doi.org/10.1038/nature07743.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  41. Maclean CJ, Metzger BPH, Yang JR, Ho WC, Moyers B, Zhang J. Deciphering the genic basis of yeast fitness variation by simultaneous forward and reverse genetics. Mol Biol Evol. 2017;34(10):2486–502.  https://doi.org/10.1093/molbev/msx151.CrossRefPubMedGoogle Scholar
  42. Marsit S, Leducq JB, Durand E, Marchant A, Filteau M, Landry CR. Evolutionary biology through the lens of budding yeast comparative genomics. Nat Rev Genet. 2017;18(10):581–98.Google Scholar
  43. McDonald MJ, Rice DP, Desai MM. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature. 2016;531(7593):233–6.  https://doi.org/10.1038/nature17143.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  44. Mora C, Tittensor DP, Adl S, Simpson AG, Worm B. How many species are there on Earth and in the ocean? PLoS Biol. 2011;9(8):e1001127.  https://doi.org/10.1371/journal.pbio.1001127.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Murphy HA, Zeyl CW. A potential case of reinforcement in a facultatively sexual unicellular eukaryote. Am Nat. 2015;186(2):312–9.  https://doi.org/10.1086/682071.CrossRefPubMedGoogle Scholar
  46. Naranjo S, Smith JD, Artieri CG, Zhang M, Zhou Y, Palmer ME, Fraser HB. Dissecting the genetic basis of a complex cis-regulatory adaptation. PLoS Genet. 2015;11(12):e1005751.  https://doi.org/10.1371/journal.pgen.1005751.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Naumov GI, Naumova ES, Sniegowski PD. Saccharomyces paradoxus and Saccharomyces cerevisiae are associated with exudates of North American oaks. Can J Microbiol. 1998;44(11):1045–50.CrossRefPubMedGoogle Scholar
  48. Newsham K, Hopkins D, Carvalhais L, Fretwell P, Rushton S, O’Donnell A, Dennis P. Relationship between soil fungal diversity and temperature in the maritime Antarctic. Nat Clim Chang. 2016;6:182–6.ADSGoogle Scholar
  49. Peris D, Langdon QK, Moriarty RV, Sylvester K, Bontrager M, Charron G, Leducq JB, Landry CR, Libkind D, Hittinger CT. Complex ancestries of lager-brewing hybrids were shaped by standing variation in the wild yeast Saccharomyces eubayanus. PLoS Genet. 2016;12(7):e1006155.  https://doi.org/10.1371/journal.pgen.1006155.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Peris D, Arias A, Orlic S, Belloch C, Perez-Traves L, Querol A, Barrio E. Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species. Mol Phylogenet Evol. 2017a;108:49–60.  https://doi.org/10.1016/j.ympev.2017.02.008.CrossRefPubMedGoogle Scholar
  51. Peris D, Moriarty RV, Alexander WG, Baker E, Sylvester K, Sardi M, Langdon QK, Libkind D, Wang QM, Bai FY, Leducq JB, Charron G, Landry CR, Sampaio JP, Goncalves P, Hyma KE, Fay JC, Sato TK, Hittinger CT. Hybridization and adaptive evolution of diverse Saccharomyces species for cellulosic biofuel production. Biotechnol Biofuels. 2017b;10:78.  https://doi.org/10.1186/s13068-017-0763-7.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Piatkowska EM, Naseeb S, Knight D, Delneri D. Chimeric protein complexes in hybrid species generate novel phenotypes. PLoS Genet. 2013;9(10):e1003836.  https://doi.org/10.1371/journal.pgen.1003836.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Presgraves DC. The molecular evolutionary basis of species formation. Nat Rev Genet. 2010;11(3):175–80.  https://doi.org/10.1038/nrg2718.CrossRefPubMedGoogle Scholar
  54. Raj A, Stephens M, Pritchard JK. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics. 2014;197(2):573–89.  https://doi.org/10.1534/genetics.114.164350.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Redzepovic S, Orlic S, Sikora S, Majdak A, Pretorius IS. Identification and characterization of Saccharomyces cerevisiae and Saccharomyces paradoxus strains isolated from Croatian vineyards. Lett Appl Microbiol. 2002;35(4):305–10.CrossRefPubMedGoogle Scholar
  56. Replansky T, Koufopanou V, Greig D, Bell G. Saccharomyces sensu stricto as a model system for evolution and ecology. Trends Ecol Evol. 2008;23(9):494–501.  https://doi.org/10.1016/j.tree.2008.05.005.CrossRefPubMedGoogle Scholar
  57. Richardson SM, Mitchell LA, Stracquadanio G, Yang K, Dymond JS, Di Carlo JE, Lee D, Huang CL, Chandrasegaran S, Cai Y, Boeke JD, Bader JS. Design of a synthetic yeast genome. Science. 2017;355(6329):1040–4.  https://doi.org/10.1126/science.aaf4557.ADSCrossRefPubMedGoogle Scholar
  58. Robinson HA, Pinharanda A, Bensasson D. Summer temperature can predict the distribution of wild yeast populations. Ecol Evol. 2016;6(4):1236–50.  https://doi.org/10.1002/ece3.1919.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Samani P, Low-Decarie E, McKelvey K, Bell T, Burt A, Koufopanou V, Landry CR, Bell G. Metabolic variation in natural populations of wild yeast. Ecol Evol. 2015;5(3):722–32.  https://doi.org/10.1002/ece3.1376.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sampaio JP, Goncalves P. Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol. 2008;74(7):2144–52.  https://doi.org/10.1128/AEM.02396-07.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Sanchez-Perez G, Mira A, Nyiro G, Pasic L, Rodriguez-Valera F. Adapting to environmental changes using specialized paralogs. Trends Genet. 2008;24(4):154–8.  https://doi.org/10.1016/j.tig.2008.01.002.CrossRefPubMedGoogle Scholar
  62. Schumer M, Rosenthal GG, Andolfatto P. How common is homoploid hybrid speciation? Evolution. 2014;68(6):1553–60.  https://doi.org/10.1111/evo.12399.CrossRefPubMedGoogle Scholar
  63. Shannon C, Rao A, Douglass S, Criddle RS. Recombination in yeast mitochondrial DNA. J Supramol Struct. 1972;1(2):145–52.  https://doi.org/10.1002/jss.400010207.CrossRefPubMedGoogle Scholar
  64. Shapira R, Levy T, Shaked S, Fridman E, David L. Extensive heterosis in growth of yeast hybrids is explained by a combination of genetic models. Heredity (Edinb). 2014;113(4):316–26.  https://doi.org/10.1038/hdy.2014.33.CrossRefGoogle Scholar
  65. Sniegowski PD, Dombrowski PG, Fingerman E. Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res. 2002;1(4):299–306.PubMedGoogle Scholar
  66. Stefanini I, Dapporto L, Legras JL, Calabretta A, Di Paola M, De Filippo C, Viola R, Capretti P, Polsinelli M, Turillazzi S, Cavalieri D. Role of social wasps in Saccharomyces cerevisiae ecology and evolution. Proc Natl Acad Sci U S A. 2012;109(33):13398–403.  https://doi.org/10.1073/pnas.1208362109.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  67. Swain Lenz D, Riles L, Fay JC. Heterochronic meiotic misexpression in an interspecific yeast hybrid. Mol Biol Evol. 2014;31(6):1333–42.  https://doi.org/10.1093/molbev/msu098.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sylvester K, Wang QM, James B, Mendez R, Hulfachor AB, Hittinger CT. Temperature and host preferences drive the diversification of Saccharomyces and other yeasts: a survey and the discovery of eight new yeast species. FEMS Yeast Res. 2015;15(3):fov002.  https://doi.org/10.1093/femsyr/fov002.CrossRefPubMedGoogle Scholar
  69. Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science. 2009;324(5927):659–62.  https://doi.org/10.1126/science.1169766.ADSCrossRefPubMedGoogle Scholar
  70. Tsai IJ, Bensasson D, Burt A, Koufopanou V. Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle. Proc Natl Acad Sci U S A. 2008;105(12):4957–62.  https://doi.org/10.1073/pnas.0707314105.ADSCrossRefPubMedPubMedCentralGoogle Scholar
  71. Turner RJ, Lovato M, Schimmel P. One of two genes encoding glycyl-tRNA synthetase in Saccharomyces cerevisiae provides mitochondrial and cytoplasmic functions. J Biol Chem. 2000;275(36):27681–8.  https://doi.org/10.1074/jbc.M003416200.PubMedGoogle Scholar
  72. Turner BC, Perkins DD, Fairfield A. Neurospora from natural populations: a global study. Fungal Genet Biol. 2001;32(2):67–92.  https://doi.org/10.1006/fgbi.2001.1247.CrossRefPubMedGoogle Scholar
  73. Wong Miller KM, Bracewell RR, Eisen MB, Bachtrog D. Patterns of genome-wide diversity and population structure in the Drosophila athabasca species complex. Mol Biol Evol. 2017;34(8):1912–23.  https://doi.org/10.1093/molbev/msx134.CrossRefPubMedGoogle Scholar
  74. Xia W, Nielly-Thibault L, Charron G, Landry CR, Kasimer D, Anderson JB, Kohn LM. Population genomics reveals structure at the individual, host-tree scale and persistence of genotypic variants of the undomesticated yeast Saccharomyces paradoxus in a natural woodland. Mol Ecol. 2017;26(4):995–1007.  https://doi.org/10.1111/mec.13954.CrossRefPubMedGoogle Scholar
  75. Yue JX, Li J, Aigrain L, Hallin J, Persson K, Oliver K, Bergstrom A, Coupland P, Warringer J, Lagomarsino MC, Fischer G, Durbin R, Liti G. Contrasting evolutionary genome dynamics between domesticated and wild yeasts. Nat Genet. 2017;49(6):913–24.  https://doi.org/10.1038/ng.3847.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Zhang H, Skelton A, Gardner RC, Goddard MR. Saccharomyces paradoxus and Saccharomyces cerevisiae reside on oak trees in New Zealand: evidence for migration from Europe and interspecies hybrids. FEMS Yeast Res. 2010;10(7):941–7.  https://doi.org/10.1111/j.1567-1364.2010.00681.x.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Mathieu Hénault
    • 1
  • Chris Eberlein
    • 1
  • Guillaume Charron
    • 1
  • Éléonore Durand
    • 1
  • Lou Nielly-Thibault
    • 1
  • Hélène Martin
    • 1
  • Christian R. Landry
    • 1
  1. 1.Département de Biologie and Département de Biochimie, Microbiologie et Bio-informatiqueInstitut de Biologie Intégrative et des Systèmes, PROTEO, Université LavalQCCanada

Personalised recommendations