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Cited by 1,117Fungal and yeast genetics researchYeasts and Rust Fungi StudiesGenetic diversity and population structure

Genome evolution across 1,011 Saccharomyces cerevisiae isolates

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Peter, Jackson, De Chiara, Matteo, Friedrich, Anne, Yue, Jia-Xing, Pflieger, David, Bergström, Anders, Sigwalt, Anastasie, Barre, Benjamin +13 more·2018·Nature
DOI 10.1038/s41586-018-0030-5PMC PMC6784862
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Abstract

Large-scale population genomic surveys are essential to explore the phenotypic diversity of natural populations. Here we report the whole-genome sequencing and phenotyping of 1,011 Saccharomyces cerevisiae isolates, which together provide an accurate evolutionary picture of the genomic variants that shape the species-wide phenotypic landscape of this yeast. Genomic analyses support a single ‘out-of-China’ origin for this species, followed by several independent domestication events. Although domesticated isolates exhibit high variation in ploidy, aneuploidy and genome content, genome evolution in wild isolates is mainly driven by the accumulation of single nucleotide polymorphisms. A common feature is the extensive loss of heterozygosity, which represents an essential source of inter-individual variation in this mainly asexual species. Most of the single nucleotide polymorphisms, including experimentally identified functional polymorphisms, are present at very low frequencies. The largest numbers of variants identified by genome-wide association are copy-number changes, which have a greater phenotypic effect than do single nucleotide polymorphisms. This resource will guide future population genomics and genotype–phenotype studies in this classic model system. Whole-genome sequencing of 1,011 natural isolates of the yeast Saccharomyces cerevisiae reveals its evolutionary history, including a single out-of-China origin and multiple domestication events, and provides a framework for genotype–phenotype studies in this model organism.

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  • Many S. cerevisiae strains contain the high-copy 2 μm plasmid (653 of 1011 sequenced S. cerevisiae strains).

    “While many S. cerevisiae strains contain the high-copy 2 µm plasmid (i.e., 653 of 1011 sequenced S. cerevisiae strains) (Peter et al. 2018)”

    From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Peter et al. 2018

    The Methods section (‘S. cerevisiae sequenced isolates’; page unavailable) confirms that 1,011 isolates were analysed. ‘Species-wide genetic and phenotypic diversity’ identifies 2μ plasmid ORFs among extreme high-copy cases, but our copy does not report that 653 isolates contained the plasmid; a search for 653 found no matching passage. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

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Research works printed but not linked: 69

  1. [1]Botstein D Fink GR Yeast: an experimental organism for 21st century biology Genetics 2011 189 695 704 10.1534/genetics.111.130765 22084421 PMC3213361 · DOI
  2. [2]Goffeau A Life with 6000 genes Science 1996 274 546 567 10.1126/science.274.5287.546 8849441 · DOI
  3. [3]Schacherer J Shapiro JA Ruderfer DM Kruglyak L Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae Nature 2009 458 342 345 10.1038/nature07670 19212320 PMC2782482 · DOI
  4. [4]Liti G Population genomics of domestic and wild yeasts Nature 2009 458 337 341 10.1038/nature07743 19212322 PMC2659681 · DOI
  5. [5]Peter J Schacherer J Population genomics of yeasts: towards a comprehensive view across a broad evolutionary scale Yeast 2016 33 73 81 10.1002/yea.3142 26592376 · DOI
  6. [6]Skelly DA Integrative phenomics reveals insight into the structure of phenotypic diversity in budding yeast Genome Res. 2013 23 1496 1504 10.1101/gr.155762.113 23720455 PMC3759725 · DOI
  7. [7]Bergström A A high-definition view of functional genetic variation from natural yeast genomes Mol. Biol. Evol 2014 31 872 888 10.1093/molbev/msu037 24425782 PMC3969562 · DOI
  8. [8]Strope PK The 100-genomes strains, an S. cerevisiae resource that illuminates its natural phenotypic and genotypic variation and emergence as an opportunistic pathogen Genome Res. 2015 25 762 774 10.1101/gr.185538.114 25840857 PMC4417123 · DOI
  9. [9]Almeida P A population genomics insight into the Mediterranean origins of wine yeast domestication Mol. Ecol. 2015 24 5412 5427 10.1111/mec.13341 26248006 · DOI
  10. [10]Zhu YO Sherlock G Petrov DA Whole genome analysis of 132 clinical Saccharomyces cerevisiae strains reveals extensive ploidy variation G3 (Bethesda) 2016 6 2421 2434 10.1534/g3.116.029397 27317778 PMC4978896 · DOI
  11. [11]Gallone B Domestication and divergence of Saccharomyces cerevisiae beer yeasts Cell 2016 166 1397 1410.e16 10.1016/j.cell.2016.08.020 27610566 PMC5018251 · DOI · Paper page
  12. [12]Gonçalves M Distinct domestication trajectories in top-fermenting beer yeasts and wine yeasts Curr. Biol 2016 26 2750 2761 10.1016/j.cub.2016.08.040 27720622 · DOI
  13. [13]The 1001 Genomes Consortium 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana Cell 2016 166 481 491 10.1016/j.cell.2016.05.063 27293186 PMC4949382 · DOI
  14. [15]Lek M Analysis of protein-coding genetic variation in 60,706 humans Nature 2016 536 285 291 10.1038/nature19057 27535533 PMC5018207 · DOI · Paper page
  15. [16]Fay JC The molecular basis of phenotypic variation in yeast Curr. Opin. Genet. Dev 2013 23 672 677 10.1016/j.gde.2013.10.005 24269094 PMC3899683 · DOI
  16. [17]Kumar P Henikoff S Ng PC Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm Nat. Protocols 2009 4 1073 1081 10.1038/nprot.2009.86 19561590 · DOI · Paper page
  17. [18]Hou J The hidden complexity of Mendelian traits across natural yeast populations Cell Reports 2016 16 1106 1114 10.1016/j.celrep.2016.06.048 27396326 PMC4963288 · DOI
  18. [19]Lippert C FaST linear mixed models for genome-wide association studies Nat. Methods 2011 8 833 835 10.1038/nmeth.1681 21892150 · DOI · Paper page
  19. [20]Ludlow CL Independent origins of yeast associated with coffee and cacao fermentation Curr. Biol. 2016 26 965 971 10.1016/j.cub.2016.02.012 27020745 PMC4821677 · DOI
  20. [21]Alexander DH Novembre J Lange K Fast model-based estimation of ancestry in unrelated individuals Genome Res. 2009 19 1655 1664 10.1101/gr.094052.109 19648217 PMC2752134 · DOI · Paper page
  21. [22]Wang QM Liu WQ Liti G Wang SA Bai FY Surprisingly diverged populations of Saccharomyces cerevisiae in natural environments remote from human activity Mol. Ecol. 2012 21 5404 5417 10.1111/j.1365-294X.2012.05732.x 22913817 · DOI
  22. [23]Borneman AR Pretorius IS Genomic insights into the Saccharomyces sensu stricto complex Genetics 2015 199 281 291 10.1534/genetics.114.173633 25657346 PMC4317643 · DOI
  23. [24]Yue JX Contrasting evolutionary genome dynamics between domesticated and wild yeasts Nat. Genet. 2017 49 913 924 10.1038/ng.3847 28416820 PMC5446901 · DOI
  24. [25]Boynton PJ Greig D The ecology and evolution of non-domesticated Saccharomyces species Yeast 2014 31 449 462 25242436 PMC4282469
  25. [26]Liti G High quality de novo sequencing and assembly of the Saccharomyces arboricolus genome BMC Genomics 2013 14 69 10.1186/1471-2164-14-69 23368932 PMC3599269 · DOI
  26. [27]Hittinger CT Remarkably ancient balanced polymorphisms in a multi-locus gene network Nature 2010 464 54 58 10.1038/nature08791 20164837 PMC2834422 · DOI
  27. [28]Hose J Dosage compensation can buffer copy-number variation in wild yeast eLife 2015 4 e05462 10.7554/eLife.05462 PMC4448642 25955966 · DOI
  28. [29]Sunshine AB The fitness consequences of aneuploidy are driven by condition-dependent gene effects PLoS Biol 2015 13 e1002155 10.1371/journal.pbio.1002155 26011532 PMC4444335 · DOI
  29. [30]Gerstein AC Chun HJ Grant A Otto SP Genomic convergence toward diploidy in Saccharomyces cerevisiae PLoS Genet 2006 2 e145 10.1371/journal.pgen.0020145 17002497 PMC1570378 · DOI
  30. [31]Zörgö E Ancient evolutionary trade-offs between yeast ploidy states PLoS Genet 2013 9 e1003388 10.1371/journal.pgen.1003388 23555297 PMC3605057 · DOI
  31. [32]Torres EM Effects of aneuploidy on cellular physiology and cell division in haploid yeast Science 2007 317 916 924 10.1126/science.1142210 17702937 · DOI · Paper page
  32. [33]Yona AH Chromosomal duplication is a transient evolutionary solution to stress Proc. Natl Acad. Sci. USA 2012 109 21010 21015 10.1073/pnas.1211150109 23197825 PMC3529009 · DOI · Paper page
  33. [34]Tan Z Aneuploidy underlies a multicellular phenotypic switch Proc. Natl Acad. Sci. USA 2013 110 12367 12372 10.1073/pnas.1301047110 23812752 PMC3725063 · DOI
  34. [35]Tettelin H Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome” Proc. Natl Acad. Sci. USA 2005 102 13950 13955 10.1073/pnas.0506758102 16172379 PMC1216834 · DOI
  35. [36]Brown CA Murray AW Verstrepen KJ Rapid expansion and functional divergence of subtelomeric gene families in yeasts Curr. Biol. 2010 20 895 903 10.1016/j.cub.2010.04.027 20471265 PMC2877759 · DOI
  36. [37]Dunn B Richter C Kvitek DJ Pugh T Sherlock G Analysis of the Saccharomyces cerevisiae pan-genome reveals a pool of copy number variants distributed in diverse yeast strains from differing industrial environments Genome Res. 2012 22 908 924 10.1101/gr.130310.111 22369888 PMC3337436 · DOI
  37. [38]Ruderfer DM Pratt SC Seidel HS Kruglyak L Population genomic analysis of outcrossing and recombination in yeast Nat. Genet. 2006 38 1077 1081 10.1038/ng1859 16892060 · DOI
  38. [39]Tsai IJ Bensasson D Burt A Koufopanou V Population genomics of the wild yeast Saccharomyces paradoxus: quantifying the life cycle Proc. Natl Acad. Sci. USA 2008 105 4957 4962 10.1073/pnas.0707314105 18344325 PMC2290798 · DOI
  39. [40]Friedrich A Jung P Reisser C Fischer G Schacherer J Population genomics reveals chromosome-scale heterogeneous evolution in a protoploid yeast Mol. Biol. Evol 2015 32 184 192 10.1093/molbev/msu295 25349286 PMC4271529 · DOI
  40. [41]Magwene PM Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae Proc. Natl Acad. Sci. USA 2011 108 1987 1992 10.1073/pnas.1012544108 21245305 PMC3033294 · DOI
  41. [42]Llorente B Smith CE Symington LS Break-induced replication: what is it and what is it for? Cell Cycle 2008 7 859 864 10.4161/cc.7.7.5613 18414031 · DOI
  42. [43]Laureau R Extensive recombination of a yeast diploid hybrid through meiotic reversion PLoS Genet 2016 12 e1005781 10.1371/journal.pgen.1005781 26828862 PMC4734685 · DOI
  43. [44]Brion C Variation of the meiotic recombination landscape and properties over a broad evolutionary distance in yeasts PLoS Genet 2017 13 e1006917 10.1371/journal.pgen.1006917 28763437 PMC5554000 · DOI
  44. [45]Ohnuki S Phenotypic diagnosis of lineage and differentiation during sake yeast breeding G3 (Bethesda) 2017 7 2807 2820 10.1534/g3.117.044099 28642365 PMC5555484 · DOI
  45. [46]Fogel S Welch JW Tandem gene amplification mediates copper resistance in yeast Proc. Natl Acad. Sci. USA 1982 79 5342 5346 10.1073/pnas.79.17.5342 6291039 PMC346892 · DOI
  46. [47]Conrad DF Origins and functional impact of copy number variation in the human genome Nature 2010 464 704 712 10.1038/nature08516 19812545 PMC3330748 · DOI · Paper page
  47. [49]Zuk O Hechter E Sunyaev SR Lander ES The mystery of missing heritability: genetic interactions create phantom heritability Proc. Natl Acad. Sci. USA 2012 109 1193 1198 10.1073/pnas.1119675109 22223662 PMC3268279 · DOI · Paper page
  48. [50]Paten B Novak AM Eizenga JM Garrison E Genome graphs and the evolution of genome inference Genome Res. 2017 27 665 676 10.1101/gr.214155.116 28360232 PMC5411762 · DOI · Paper page
  49. [51]Luo R SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler Gigascience 2012 1 18 10.1186/2047-217X-1-18 23587118 PMC3626529 · DOI
  50. [53]McKenna A The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data Genome Res. 2010 20 1297 1303 10.1101/gr.107524.110 20644199 PMC2928508 · DOI · Paper page
  51. [54]Cingolani P A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3 Fly (Austin) 2012 6 80 92 10.4161/fly.19695 22728672 PMC3679285 · DOI · Paper page
  52. [55]Simpson JT ABySS: a parallel assembler for short read sequence data Genome Res. 2009 19 1117 1123 10.1101/gr.089532.108 19251739 PMC2694472 · DOI
  53. [56]Otto TD Dillon GP Degrave WS Berriman M RATT: rapid annotation transfer tool Nucleic Acids Res 2011 39 e57 10.1093/nar/gkq1268 21306991 PMC3089447 · DOI
  54. [57]Proux-Wéra E Armisén D Byrne KP Wolfe KH A pipeline for automated annotation of yeast genome sequences by a conserved-synteny approach BMC Bioinformatics 2012 13 237 10.1186/1471-2105-13-237 22984983 PMC3507789 · DOI
  55. [58]Holt C Yandell M MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects BMC Bioinformatics 2011 12 491 10.1186/1471-2105-12-491 22192575 PMC3280279 · DOI
  56. [59]Haas BJ Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments Genome Biol. 2008 9 R7 10.1186/gb-2008-9-1-r7 18190707 PMC2395244 · DOI
  57. [60]Scannell DR The awesome power of yeast evolutionary genetics: new genome sequences and strain resources for the Saccharomyces sensu stricto genus G3 (Bethesda) 2011 1 11 25 10.1534/g3.111.000273 22384314 PMC3276118 · DOI
  58. [61]Baker E The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts Mol. Biol. Evol. 2015 32 2818 2831 10.1093/molbev/msv168 26269586 PMC4651232 · DOI
  59. [62]Hittinger CT Genomics and the making of yeast biodiversity Curr. Opin. Genet. Dev 2015 35 100 109 10.1016/j.gde.2015.10.008 26649756 PMC4771062 · DOI
  60. [63]Yang Z PAML 4: phylogenetic analysis by maximum likelihood Mol. Biol. Evol. 2007 24 1586 1591 10.1093/molbev/msm088 17483113 · DOI · Paper page
  61. [64]Hutter S Vilella AJ Rozas J Genome-wide DNA polymorphism analyses using VariScan BMC Bioinformatics 2006 7 409 10.1186/1471-2105-7-409 16968531 PMC1574356 · DOI
  62. [65]Chang CC Second-generation PLINK: rising to the challenge of larger and richer datasets Gigascience 2015 4 7 10.1186/s13742-015-0047-8 25722852 PMC4342193 · DOI · Paper page
  63. [66]Danecek P The variant call format and VCFtools Bioinformatics 2011 27 2156 2158 10.1093/bioinformatics/btr330 21653522 PMC3137218 · DOI
  64. [67]Istace B de novo assembly and population genomic survey of natural yeast isolates with the Oxford Nanopore MinION sequencer Gigascience 2017 6 1 13 10.1093/gigascience/giw018 PMC5466710 28369459 · DOI
  65. [68]Lechner M Proteinortho: detection of (co-)orthologs in large-scale analysis BMC Bioinformatics 2011 12 124 10.1186/1471-2105-12-124 21526987 PMC3114741 · DOI
  66. [69]Edgar RC MUSCLE: a multiple sequence alignment method with reduced time and space complexity BMC Bioinformatics 2004 5 113 10.1186/1471-2105-5-113 15318951 PMC517706 · DOI
  67. [70]Suyama M Torrents D Bork P PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments Nucleic Acids Res 2006 34 W609 W612 10.1093/nar/gkl315 16845082 PMC1538804 · DOI
  68. [71]Mirarab S ASTRAL: genome-scale coalescent-based species tree estimation Bioinformatics 2014 30 i541 i548 10.1093/bioinformatics/btu462 25161245 PMC4147915 · DOI
  69. [72]Wagih O Parts L Gitter: a robust and accurate method for quantification of colony sizes from plate images G3 (Bethesda) 2014 4 547 552 10.1534/g3.113.009431 24474170 PMC3962492 · DOI

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Authors
Peter, J., De Chiara, M., Friedrich, A., Yue, J.-X., Pflieger, D., Bergström, A., Sigwalt, A., Barre, B., Freel, K., Llored, A., Cruaud, C., Labadie, K., Aury, J.-M., Istace, B., Lebrigand, K., Barbry, P., Engelen, S., Lemainque, A., Wincker, P., Liti, G., & Schacherer, J.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
Corresponding author
  • Liti, Gianni
  • Schacherer, Joseph
ORCID
Venue
Nature
Publisher
Springer Science and Business Media LLC
Published
2018-04
Volume
556
Issue
7701
Pages
339-344
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
DOI
10.1038/s41586-018-0030-5
PMC
PMC6784862
OpenAlex
W2798064943
Cited by
1,117
References
3
Citations by year
2026: 119 · 2025: 117 · 2024: 132 · 2023: 131 · 2022: 151 · 2021: 146 · 2020: 135 · 2019: 140 · 2018: 45
FWCI
41.45
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • RePEc: Research Papers in Economics (submittedVersion)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
Funders
  • Science Foundation Ireland
  • Agence Nationale de la Recherche (10-INBS-09-08, ANR-16-CE12-0019, ANR-10-INBS-0009, ANR- 10-INBS-09, ANR 10-INBS-09-08, ANR-10, ANR-13-BSV6-0006, ANR-16-CE12, ANR-11-LABX-0057, 10-INBS-09, ANR-11-LABX-0028)
  • Institut National de la Santé et de la Recherche Médicale (ANR-11-LABX-0028-01)
  • Université de Strasbourg
  • Fondation ARC pour la Recherche sur le Cancer (#ANR-11-LABX-0028-01, SFI 20111203947, PDF20150602803)
  • Ligue Contre le Cancer (ANR-10-INBS-09-08, ANR-11-LABX-0028-01, GB-MA-CD-11287)
  • Centre National de la Recherche Scientifique (ANR-11-LABX-0028-01)
  • Institut Universitaire de France
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM101091)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
Keywords
Saccharomyces cerevisiae, genome evolution, population genomics, domestication, single nucleotide polymorphisms, loss of heterozygosity, copy number variation, genome-wide association study, ploidy variation, aneuploidy, genotype-phenotype mapping, natural yeast isolates, asexual reproduction
MeSH terms
Alleles, Aneuploidy, China, Phenotype, Phylogeny, Ploidies, Saccharomyces cerevisiae, Genetic Variation, Genome, Fungal, Sequence Analysis, DNA, Evolution, Molecular, Loss of Heterozygosity, Polymorphism, Single Nucleotide, Genomics, Genome-Wide Association Study, Genetic Association Studies, DNA Copy Number Variations, Phylogeography

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