1887

Abstract

Interspecific hybridization has played an important role in the evolution of eukaryotic organisms by favouring genetic interchange between divergent lineages to generate new phenotypic diversity involved in the adaptation to new environments. This way, hybridization between species, involving the fusion between their metabolic capabilities, is a recurrent adaptive strategy in industrial environments. In the present study, whole-genome sequences of natural hybrids between and were obtained to unveil the mechanisms involved in the origin and evolution of hybrids, as well as the ecological and geographic contexts in which spontaneous hybridization and hybrid persistence take place. Although species can mate using different mechanisms, we concluded that rare-mating is the most commonly used, but other mechanisms were also observed in specific hybrids. The preponderance of rare-mating was confirmed by performing artificial hybridization experiments. The mechanism used to mate determines the genomic structure of the hybrid and its final evolutionary outcome. The evolution and adaptability of the hybrids are triggered by genomic instability, resulting in a wide diversity of genomic rearrangements. Some of these rearrangements could be adaptive under the stressful conditions of the industrial environment.

Funding
This study was supported by the:
  • Ministerio de Ciencia, Innovación y Universidades (Award JCI-2012-14056)
    • Principle Award Recipient: Christina Toft
  • Consejo Nacional de Ciencia y Tecnología (Award 176060)
    • Principle Award Recipient: Guadalupe Ortiz-Tovar
  • Conselleria d'Educació, Investigació, Cultura i Esport (Award ACIF/2015/194)
    • Principle Award Recipient: Miguel Morard
  • Ministerio de Ciencia, Innovación y Universidades (Award RTI2018-093744-B-C32)
    • Principle Award Recipient: Eladio Barrio
  • Ministerio de Ciencia, Innovación y Universidades (Award RTI2018-093744-B-C31)
    • Principle Award Recipient: Amparo Querol
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000333
2020-02-17
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/3/mgen000333.html?itemId=/content/journal/mgen/10.1099/mgen.0.000333&mimeType=html&fmt=ahah

References

  1. Harrison RG. Hybrids and hybrid zones: historical perspective. In Harrison RG. editor Hybrid Zones and the Evolutionary Process Oxford, U.K: Oxford University Press; 1993 pp 3–12
    [Google Scholar]
  2. Bell M, Travis M. Hybridization, transgressive segregation, genetic covariation, and adaptive radiation. Trends Ecol Evol 2005; 20:358–361 [View Article]
    [Google Scholar]
  3. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE et al. Hybridization and speciation. J Evol Biol 2013; 26:229–246 [View Article]
    [Google Scholar]
  4. Arnold ML. Natural Hybridization and Evolution, 1 ed. Cary, NC, USA: Oxford University Press; 1997
    [Google Scholar]
  5. Gérard PR, Alix K, Heslop-Harrison JS, Schwarzacher T. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 2017; 120:183–194
    [Google Scholar]
  6. Goulet BE, Roda F, Hopkins R. Hybridization in plants: old ideas, new techniques. Plant Physiol 2017; 173:65–78 [View Article]
    [Google Scholar]
  7. Yakimowski SB, Rieseberg LH. The role of homoploid hybridization in evolution: a century of studies synthesizing genetics and ecology. Am J Bot 2014; 101:1247–1258 [View Article]
    [Google Scholar]
  8. Mavárez J, Linares M. Homoploid hybrid speciation in animals. Mol Ecol 2008; 17:4181–4185 [View Article]
    [Google Scholar]
  9. Dowling TE, Secor CL. The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 1997; 28:593–619 [View Article]
    [Google Scholar]
  10. Ackermann RR, Arnold ML, Baiz MD, Cahill JA, Cortés‐Ortiz L et al. Hybridization in human evolution: insights from other organisms. Evol Anthropol 2019; 28:189–209 [View Article]
    [Google Scholar]
  11. Stukenbrock EH. The role of hybridization in the evolution and emergence of new fungal plant pathogens. Phytopathology 2016; 106:104–112 [View Article]
    [Google Scholar]
  12. Depotter JRL, Seidl MF, Wood TA, Thomma BPHJ. Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Curr Opin Microbiol 2016; 32:7–13 [View Article]
    [Google Scholar]
  13. Peris D, Pérez-Torrado R, Hittinger CT, Barrio E, Querol A. On the origins and industrial applications of Saccharomyces cerevisiae × Saccharomyces kudriavzevii hybrids. Yeast 2018; 35:51–69 [View Article]
    [Google Scholar]
  14. Morales L, Dujon B. Evolutionary role of interspecies hybridization and genetic exchanges in yeasts. Microbiol Mol Biol Rev 2012; 76:721–739 [View Article]
    [Google Scholar]
  15. Sipiczki M. Interspecies hybridization and recombination in Saccharomyces wine yeasts. FEMS Yeast Res 2008; 8:996–1007 [View Article]
    [Google Scholar]
  16. Sipiczki M. Interspecies hybridisation and genome chimerisation in Saccharomyces combining of gene pools of species and its biotechnological perspectives. Front Microbiol 2018; 9:3071 [View Article]
    [Google Scholar]
  17. Pérez-Través L, Lopes CA, Querol A, Barrio E. On the complexity of the Saccharomyces bayanus taxon: hybridization and potential hybrid speciation. PLoS One 2014; 9:e93729 [View Article]
    [Google Scholar]
  18. Ortiz-Merino RA, Kuanyshev N, Braun-Galleani S, Byrne KP, Porro D et al. Evolutionary restoration of fertility in an interspecies hybrid yeast, by whole-genome duplication after a failed mating-type switch. PLoS Biol 2017; 15:e2002128 [View Article]
    [Google Scholar]
  19. Lopandic K. Saccharomyces interspecies hybrids as model organisms for studying yeast adaptation to stressful environments. Yeast 2018; 35:21–38 [View Article]
    [Google Scholar]
  20. Eberlein C, Hénault M, Fijarczyk A, Charron G, Bouvier M et al. Hybridization is a recurrent evolutionary stimulus in wild yeast speciation. Nat Commun 2019; 10:923 [View Article]
    [Google Scholar]
  21. Greig D, Louis EJ, Borts RH, Travisano M. Hybrid speciation in experimental populations of yeast. Science 2002; 298:1773–1775 [View Article]
    [Google Scholar]
  22. Stelkens RB, Brockhurst MA, Hurst GDD, Miller EL, Greig D. The effect of hybrid transgression on environmental tolerance in experimental yeast crosses. J Evol Biol 2014; 27:2507–2519 [View Article]
    [Google Scholar]
  23. Boynton PJ, Greig D. The ecology and evolution of non-domesticated Saccharomyces species. Yeast 2014; 31:449–462
    [Google Scholar]
  24. Naseeb S, James SA, Alsammar H, Michaels CJ, Gini B et al. Saccharomyces jurei sp. nov., isolation and genetic identification of a novel yeast species from Quercus robur . Int J Syst Evol Microbiol 2017; 67:2046–2052 [View Article]
    [Google Scholar]
  25. Hittinger CT. Saccharomyces diversity and evolution: a budding model genus. Trends Genet 2013; 29:309–317 [View Article]
    [Google Scholar]
  26. Greig D. Reproductive isolation in Saccharomyces . Heredity 2008
    [Google Scholar]
  27. Pérez-Través L, Lopes CA, Barrio E, Querol A. Evaluation of different genetic procedures for the generation of artificial hybrids in Saccharomyces genus for winemaking. Int J Food Microbiol 2012; 156:102–111 [View Article]
    [Google Scholar]
  28. Naumov GI. Genetic identification of biological species in the Saccharomyces sensu stricto complex. J Ind Microbiol 1996; 17:295–302
    [Google Scholar]
  29. Stefanini I, Dapporto L, Berná L, Polsinelli M, Turillazzi S et al. Social wasps are a Saccharomyces mating nest. Proc Natl Acad Sci USA 2016; 113:2247–2251 [View Article]
    [Google Scholar]
  30. Pulvirenti A, Zambonelli C, Todaro A, Giudici P. Interspecific hybridisation by digestive tract of invertebrates as a source of environmental biodiversity within the Saccharomyces cerevisiae . Ann Microbiol 2002; 52:245–255
    [Google Scholar]
  31. Liti G, Barton DBH, Louis EJ, diversity S. reproductive isolation and species concepts in Saccharomyces . Genetics 2006; 174:839–850 [View Article]
    [Google Scholar]
  32. Kodama Y, Kielland-Brandt MC, Hansen J. Lager brewing yeast. In Sunnerhagen P, Piškur J. (editors) Comparative Genomics: using fungi as models (Topics in Current Genetics) Berlin, Germany: Springer-Verlag; 2005 pp 145–164
    [Google Scholar]
  33. Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J et al. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci USA 2011; 108:14539–14544 [View Article]
    [Google Scholar]
  34. Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB et al. Evidence of natural hybridization in Brazilian wild lineages of Saccharomyces cerevisiae . Genome Biol Evol 2016; 8:317–329 [View Article]
    [Google Scholar]
  35. Peter J, De Chiara M, Friedrich A, Yue J-X, Pflieger D et al. Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature 2018; 556:339–344 [View Article]
    [Google Scholar]
  36. Pontes A, Čadež N, Gonçalves P, Sampaio JP. A quasi-domesticate relic hybrid population of Saccharomyces cerevisiae × S. paradoxus adapted to olive brine. Front Genet 2019; 10:449 [View Article]
    [Google Scholar]
  37. 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; 10:941–947 [View Article]
    [Google Scholar]
  38. Almeida P, Gonçalves C, Teixeira S, Libkind D, Bontrager M et al. A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum . Nat Commun 2014; 5:4044 [View Article]
    [Google Scholar]
  39. Guillamón JM, Barrio E. Genetic polymorphism in wine yeasts: mechanisms and methods for its detection. Front Microbiol 2017; 8:806 [View Article]
    [Google Scholar]
  40. Peris D, Arias A, Orlić S, Belloch C, Pérez-Través L et al. Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species. Mol Phylogenet Evol 2017; 108:49–60 [View Article]
    [Google Scholar]
  41. Krogerus K, Preiss R, Gibson B. A unique Saccharomyces cerevisiae × Saccharomyces uvarum hybrid isolated from Norwegian Farmhouse beer: characterization and reconstruction. Front Microbiol 2018; 9: [View Article]
    [Google Scholar]
  42. Gibson BR, Storgårds E, Krogerus K, Vidgren V. Comparative physiology and fermentation performance of Saaz and Frohberg lager yeast strains and the parental species Saccharomyces eubayanus . Yeast 2013; 30:255–266 [View Article]
    [Google Scholar]
  43. Ortiz-Tovar G, Pérez-Torrado R, Adam AC, Barrio E, Querol A. A comparison of the performance of natural hybrids Saccharomyces cerevisiae × Saccharomyces kudriavzevii at low temperatures reveals the crucial role of their S. kudriavzevii genomic contribution. Int J Food Microbiol 2018; 274:12–19 [View Article]
    [Google Scholar]
  44. Belloch C, Orlic S, Barrio E, Querol A. Fermentative stress adaptation of hybrids within the Saccharomyces sensu stricto complex. Int J Food Microbiol 2008; 122:188–195 [View Article]
    [Google Scholar]
  45. Pérez-Torrado R, González SS, Combina M, Barrio E, Querol A. Molecular and enological characterization of a natural Saccharomyces uvarum and Saccharomyces cerevisiae hybrid. Int J Food Microbiol 2015; 204:101–110 [View Article]
    [Google Scholar]
  46. Pfliegler WP, Atanasova L, Karanyicz E, Sipiczki M, Bond U et al. Generation of new genotypic and phenotypic features in artificial and natural yeast hybrids. Food Technol Biotechnol 2014; 52:46–57
    [Google Scholar]
  47. Hebly M, Brickwedde A, Bolat I, Driessen MRM, de Hulster EAF et al. S. cerevisiae × S. eubayanus interspecific hybrid, the best of both worlds and beyond. FEMS Yeast Res 2015; 15:fov005 [View Article]
    [Google Scholar]
  48. García-Ríos E, Guillén A, de la Cerda R, Pérez-Través L, Querol A et al. Improving the cryotolerance of wine yeast by interspecific hybridization in the genus Saccharomyces . Front Microbiol 2019; 9: [View Article]
    [Google Scholar]
  49. Krogerus K, Magalhães F, Vidgren V, Gibson B. New lager yeast strains generated by interspecific hybridization. J Ind Microbiol Biotechnol 2015; 42:769–778 [View Article]
    [Google Scholar]
  50. Pérez-Torrado R, Barrio E, Querol A. Alternative yeasts for winemaking: Saccharomyces non- cerevisiae and its hybrids. Crit Rev Food Sci Nutr 2018; 58:1780–1790 [View Article]
    [Google Scholar]
  51. Peris D, Lopes CA, Belloch C, Querol A, Barrio E. Comparative genomics among Saccharomyces cerevisiae × Saccharomyces kudriavzevii natural hybrid strains isolated from wine and beer reveals different origins. BMC Genomics 2012; 13:407 [View Article]
    [Google Scholar]
  52. Peris D, Lopes CA, Arias A, Barrio E. Reconstruction of the evolutionary history of Saccharomyces cerevisiae x S. kudriavzevii hybrids based on multilocus sequence analysis. PLoS One 2012; 7:e45527 [View Article]
    [Google Scholar]
  53. Querol A, Barrio E, Huerta T, Ramón D. Molecular monitoring of wine fermentations conducted by active dry yeast strains. Appl Environ Microbiol 1992; 58:2948–2953 [View Article]
    [Google Scholar]
  54. Morard M, Macías LG, Adam AC, Lairón-Peris M, Pérez-Torrado R et al. Aneuploidy and ethanol tolerance in Saccharomyces cerevisiae . Front Genet 2019; 10:82 [View Article]
    [Google Scholar]
  55. Macías LG, Morard M, Toft C, Barrio E. Comparative genomics between Saccharomyces kudriavzevii and S. cerevisiae applied to identify mechanisms involved in adaptation. Front Genet 2019; 10:187 [View Article]
    [Google Scholar]
  56. Joshi NA, Fass JN. Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files version 1.33. https://github.com/najoshi/sickle ; 2011
  57. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18:821–829 [View Article]
    [Google Scholar]
  58. Dayarian A, Michael TP, Sengupta AM. SOPRA: scaffolding algorithm for paired reads via statistical optimization. BMC Bioinformatics 2010; 11:345 [View Article]
    [Google Scholar]
  59. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article]
    [Google Scholar]
  60. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol 2012; 13:R56 [View Article]
    [Google Scholar]
  61. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M et al. Versatile and open software for comparing large genomes. Genome Biol 2004; 5:R12 [View Article]
    [Google Scholar]
  62. Otto TD, Dillon GP, Degrave WS, Berriman M. RATT: rapid annotation transfer tool. Nucleic Acids Res 2011; 39:e57 [View Article]
    [Google Scholar]
  63. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 2005; 33:W465–W467 [View Article]
    [Google Scholar]
  64. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16:944–945 [View Article]
    [Google Scholar]
  65. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article]
    [Google Scholar]
  66. Homer N, Merriman B, Nelson SF. BFAST: an alignment tool for large scale genome resequencing. PLoS One 2009; 4:e7767 [View Article]
    [Google Scholar]
  67. Hung J-H, Weng Z. Sequence alignment and homology search with blast and ClustalW. Cold Spring Harb Protoc 2016; 2016:pdb.prot093088 [View Article]
    [Google Scholar]
  68. Wickham H. Ggplot2: Elegant Graphics for Data Analysis Berlin, Germany: Springer; 2009
    [Google Scholar]
  69. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article]
    [Google Scholar]
  70. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article]
    [Google Scholar]
  71. Bryant D, Moulton V. Neighbor-Net: an Agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 2004; 21:255–265 [View Article]
    [Google Scholar]
  72. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article]
    [Google Scholar]
  73. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000; 155:
    [Google Scholar]
  74. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005; 14:2611–2620 [View Article]
    [Google Scholar]
  75. Earl DA, vonHoldt BM. Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 2012; 4:359–361 [View Article]
    [Google Scholar]
  76. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 2007; 23:1801–1806 [View Article]
    [Google Scholar]
  77. Ramasamy R, Ramasamy S, Bindroo B, Naik V. Structure plot: a program for drawing elegant structure bar plots in user friendly interface. Springerplus 2014; 3:431 [View Article]
    [Google Scholar]
  78. Fay JC, Liu P, Ong GT, Dunham MJ, Cromie GA et al. A polyploid admixed origin of beer yeasts derived from European and Asian wine populations. PLoS Biol 2019; 17:e3000147 [View Article]
    [Google Scholar]
  79. Huxley C, Green ED, Dunbam I. Rapid assessment of S. cerevisiae mating type by PCR. Trends Genet 1990; 6:236
    [Google Scholar]
  80. Jansen G, Wu C, Schade B, Thomas DY, Whiteway M. Drag&Drop cloning in yeast. Gene 2005; 344:43–51
    [Google Scholar]
  81. Taxis C, Knop M. System of centromeric, episomal, and integrative vectors based on drug resistance markers for Saccharomyces cerevisiae . BioTechniques 2006; 40:73–78 [View Article]
    [Google Scholar]
  82. Gietz RD. Yeast transformation by the LiAc/SS carrier DNA/PEG method. In Smith JS, Burke DJ. (editors) Yeast Genetics: Methods and Protocols New York, NY: Springer New York; 2014 pp 1–12
    [Google Scholar]
  83. Spencer JFT, Spencer DM. Rare-mating and cytoduction in Saccharomyces cerevisiae . In Evans I. editor Methods in Molecular Biology: Yeast protocols Totowa, New Jersey: Humana Press Inc; 1996 pp 39–44
    [Google Scholar]
  84. González SS, Barrio E, Querol A. Molecular characterization of new natural hybrids between Saccharomyces cerevisiae and S. kudriavzevii in brewing. Appl Environ Microbiol 2008; 74:2314–2320 [View Article]
    [Google Scholar]
  85. Gallone B, Steensels J, Prahl T, Soriaga L, Saels V et al. Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 2016; 166:e13161397–1410 [View Article]
    [Google Scholar]
  86. Liti G, Carter DM, Moses AM, Warringer J, Parts L et al. Population genomics of domestic and wild yeasts. Nature 2009; 458:337–341 [View Article]
    [Google Scholar]
  87. Legras J-L, Galeote V, Bigey F, Camarasa C, Marsit S et al. Adaptation of S. cerevisiae to fermented food environments reveals remarkable genome plasticity and the footprints of domestication. Mol Biol Evol 2018; 35:1712–1727 [View Article]
    [Google Scholar]
  88. Cross F, Hartwell LH, Jackson C, Konopka JB. Conjugation in Saccharomyces cerevisiae . Annu Rev Cell Biol 1988; 4:429–455 [View Article]
    [Google Scholar]
  89. Magwene PM, Kayıkçı Ö, Granek JA, Reininga JM, Scholl Z et al. Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae . Proc Natl Acad Sci USA 2011; 108:1987–1992 [View Article]
    [Google Scholar]
  90. Magwene PM. Revisiting Mortimer’s genome renewal hypothesis: heterozygosity, homothallism, and the potential for adaptation in yeast. In Landry CR, Aubin-Horth N. (editors) Ecological Genomics: Ecology and the Evolution of Genes and Genomes (Advances in Experimental Medicine and Biology Dordrecht, The Netherlands: Springer Netherlands; 2014 pp 37–48
    [Google Scholar]
  91. Pomper S, Daniels KM, McKee DW. Genetic analysis of polyploid yeast. Genetics 1954; 39:343–355
    [Google Scholar]
  92. Gunge N, Nakatomi Y. Genetic mechanisms of rare matings of the yeast Saccharomyces cerevisiae heterozygous for mating type. Genetics 1972; 70:58
    [Google Scholar]
  93. Kumaran R, Yang SY, Leu JY. Characterization of chromosome stability in diploid, polyploid and hybrid yeast cells. PLoS One 2013; 8:e68094 [View Article]
    [Google Scholar]
  94. Feurtey A, Stukenbrock EH. Interspecific gene exchange as a driver of adaptive evolution in fungi. Annu Rev Microbiol 2018; 72:377–398 [View Article]
    [Google Scholar]
  95. Payseur BA, Rieseberg LH. A genomic perspective on hybridization and speciation. Mol Ecol 2016; 25:2337–2360 [View Article]
    [Google Scholar]
  96. Vaughan-Martini A, Kurtzman CP. Deoxyribonucleic acid relatedness among species of the genus Saccharomyces sensu stricto. Int J Syst Bacteriol 1985; 35:508–511 [View Article]
    [Google Scholar]
  97. Nilsson-Tillgren T, Gjermansen C, Kielland-Brandt MC, Petersen JGL, Holmberg S. Genetic differences between Saccharomyces carlsbergensis and S. cerevisiae. Analysis of chromosome III by single chromosome transfer. Carlsberg Res Commun 1981; 46:65–76 [View Article]
    [Google Scholar]
  98. Gonçalves M, Pontes A, Almeida P, Barbosa R, Serra M et al. Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts. Curr Biol 2016; 26:2750–2761 [View Article]
    [Google Scholar]
  99. Monerawela C, Bond U. Brewing up a storm: the genomes of lager yeasts and how they evolved. Biotechnol Adv 2017; 35:512–519 [View Article]
    [Google Scholar]
  100. Erny C, Raoult P, Alais A, Butterlin G, Delobel P et al. Ecological success of a group of Saccharomyces cerevisiae/Saccharomyces kudriavzevii hybrids in the Northern European wine making environment. Appl Environ Microbiol 2012; 78:3256–3265 [View Article]
    [Google Scholar]
  101. Borneman AR, Forgan AH, Kolouchova R, Fraser JA, Schmidt SA. Whole Genome Comparison Reveals High Levels of Inbreeding and Strain Redundancy Across the Spectrum of Commercial Wine Strains of Saccharomyces cerevisiae . G3 2016; 6:957–971 [View Article]
    [Google Scholar]
  102. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH et al. The genome sequence of the wine yeast VIN7 reveals an allotriploid hybrid genome with Saccharomyces cerevisiae and Saccharomyces kudriavzevii origins. FEMS Yeast Res 2012; 12:88–96 [View Article]
    [Google Scholar]
  103. Tilakaratna V, Bensasson D. Habitat predicts levels of genetic admixture in Saccharomyces cerevisiae . G3 2017
    [Google Scholar]
  104. Naumov GI, Naumova ES, Masneuf I, Aigle M, Kondratieva VI et al. Natural polyploidization of some cultured yeast Saccharomyces sensu stricto: Auto- and allotetraploidy. Syst Appl Microbiol 2000; 23:442–449 [View Article]
    [Google Scholar]
  105. Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison JSP. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 2017; 120:183–194 [View Article]
    [Google Scholar]
  106. Charron G, Marsit S, Hénault M, Martin H, Landry CR. Spontaneous whole-genome duplication restores fertility in interspecific hybrids. Nat Commun 2019; 10:4126 [View Article]
    [Google Scholar]
  107. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH et al. Whole-Genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 2011; 7:e1001287 [View Article]
    [Google Scholar]
  108. Peris D, Sylvester K, Libkind D, Gonçalves P, Sampaio JP et al. Population structure and reticulate evolution of Saccharomyces eubayanus and its lager-brewing hybrids. Mol Ecol 2014; 23:2031–2045 [View Article]
    [Google Scholar]
  109. Dion-Côté A-M, Barbash DA. Beyond speciation genes: an overview of genome stability in evolution and speciation. Curr Opin Genet Dev 2017; 47:17–23 [View Article]
    [Google Scholar]
  110. Puig S, Querol A, Barrio E, Pérez-Ortín JE. Mitotic recombination and genetic changes in Saccharomyces cerevisiae during wine fermentation. Appl Environ Microbiol 2000; 66:2057–2061 [View Article]
    [Google Scholar]
  111. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G et al. Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genet 2013; 9:e1003366 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000333
Loading
/content/journal/mgen/10.1099/mgen.0.000333
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error