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Population genomics of domestic and wild yeasts

Nature volume 458, pages 337–341 (2009)Cite this article

Abstract

Since the completion of the genome sequence of Saccharomyces cerevisiae in 1996 (refs 1, 2), there has been a large increase in complete genome sequences, accompanied by great advances in our understanding of genome evolution. Although little is known about the natural and life histories of yeasts in the wild, there are an increasing number of studies looking at ecological and geographic distributions3,4, population structure5,6,7,8 and sexual versus asexual reproduction9,10. Less well understood at the whole genome level are the evolutionary processes acting within populations and species that lead to adaptation to different environments, phenotypic differences and reproductive isolation. Here we present one- to fourfold or more coverage of the genome sequences of over seventy isolates of the baker’s yeast S. cerevisiae and its closest relative, Saccharomyces paradoxus. We examine variation in gene content, single nucleotide polymorphisms, nucleotide insertions and deletions, copy numbers and transposable elements. We find that phenotypic variation broadly correlates with global genome-wide phylogenetic relationships. S. paradoxus populations are well delineated along geographic boundaries, whereas the variation among worldwide S. cerevisiae isolates shows less differentiation and is comparable to a single S. paradoxus population. Rather than one or two domestication events leading to the extant baker’s yeasts, the population structure of S. cerevisiae consists of a few well-defined, geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for cross-breeding and production of new combinations of pre-existing variations.

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Figure 1: Saccharomyces phylogenomics.
Figure 2: Saccharomyces population structure.
Figure 3: Population genomics: variation and selection.
Figure 4: Saccharomyces phenotype variation.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

ABI data were submitted to the NCBI Trace Archive (accession numbers: TI1250539685 –TI1250559725, TI1253231395–TI1253251114, TI1253289161–TI1253346699, TI1253412335–TI1253476299, TI1253519268–TI1253585710, TI1253601045–TI1253652620, TI1253786059 –TI1253860555, TI1253882296–TI1253926729, TI1253930843–TI1253993129, TI1253998006–TI1254046664, TI1254080659 –TI1254150525, TI1254155855 –TI1254203444, TI1254229054 –TI1254316243, TI1254369656 –TI1254427407, TI1254441246 –TI1254496019, TI1254545851 –TI1254582436. The Solexa data were submitted to the European Read Archive (accession number ERA000011).

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Acknowledgements

We thank all the members of the Sanger sequencing production teams for generating the sequence data. We thank members of the Durbin and Louis laboratories and C. Nieduszynski for comments and suggestions, L. Kruglyak and J. Schacherer for sharing their unpublished manuscript and R. Ames and S. Lovell for sharing unpublished results. We also thank the British Council and Chinese Academy of Sciences for providing the opportunity to design and develop this project. Research at the Wellcome Trust Sanger Institute (D.M.C., A.M.M., L.P, M.J., M.A.Q., I.G., S.S., F.S. and R.D.) is supported by The Wellcome Trust. G.L., D.B.H.B., E.B. and E.J.L. were supported by the Wellcome Trust, the Royal Society and the Biotechnology and Biological Sciences Research Council (BBSRC). S.A.J., R.P.D. and I.N.R. were supported by the BBSRC. A.B. and J.W. were supported by the Swedish Research Council and the Swedish Foundation for Strategic Research. A.B. and V.K. were supported by the National Environment Research Council (NERC) and I.J.T. was supported by the Wellcome Trust. D.B. was supported by NERC. A.M.M. was supported by the Canada Foundation for Innovation. M.J.T.O. and A.v.O. were supported by the National Science Foundation, the National Institutes of Health and a Hertz fellowship.

Author Contributions R.D. and E.J.L. designed the project. G.L. selected and manipulated yeast strains and extracted DNA samples. M.J., M.A.Q., I.G., S.S. and F.S. performed the subcloning and sequencing. D.M.C. did the reference comparison and assembly of the sequences. D.M.C. and G.L. coordinated the collection of data. D.M.C. and R.D. performed much of the global analysis, which was the basis for specific analyses performed by the other authors. A.M.M. did the selection studies. E.J.L., G.L., D.M.C. R.D., D.B.H.B., E.B. and L.P. did the population structure and analysis of new genes. C.M.B. and D.B. performed the analysis of Ty-element abundance. S.A.J., R.P.D., M.J.T.O., A.v.O. and I.N.R. analysed the rDNA. A.B., V.K. and I.J.T. did the sequence variation and recombination analyses. A.M.M. and A.N.N.B. created a BLAST server. J.W. and A.B. generated the phenomics data. E.J.L. and G.L. wrote the paper, coordinating the contributions of the other authors.

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Author notes

  1. Ian Goodhead

    Present address: Present address: School of Biological Sciences, University of Liverpool, Liverpool LG9 3BX, UK.,

  2. Gianni Liti, David M. Carter, Richard Durbin and Edward J. Louis: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Genetics, Queen’s Medical Centre, University of Nottingham, Nottingham NG7 2UH, UK

    Gianni Liti, David B. H. Barton, Elizabeth Bailes & Edward J. Louis

  2. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1HH, UK,

    David M. Carter, Alan M. Moses, Leopold Parts, Matthew Jones, Michael A. Quail, Ian Goodhead, Sarah Sims, Frances Smith & Richard Durbin

  3. Department of Cell & Systems Biology, University of Toronto, Ontario M5S 2J4, Canada

    Alan M. Moses & Alex N. Nguyen

  4. Department of Cell and Molecular Biology, Lundberg Laboratory, University of Gothenburg, Medicinaregatan 9c, 41390 Gothenburg, Sweden,

    Jonas Warringer & Anders Blomberg

  5. National Collection of Yeast Cultures, Institute of Food Research, Norwich Research Park, Colney, Norwich NR4 7UA, UK,

    Stephen A. James, Robert P. Davey & Ian N. Roberts

  6. Division of Biology, Imperial College London, Silwood Park, Ascot SL5 7PY, UK,

    Austin Burt, Vassiliki Koufopanou & Isheng J. Tsai

  7. Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, UK

    Casey M. Bergman & Douda Bensasson

  8. Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA,

    Michael J. T. O’Kelly & Alexander van Oudenaarden

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  1. Gianni Liti
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Corresponding authors

Correspondence to Richard Durbin or Edward J. Louis.

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Liti, G., Carter, D., Moses, A. et al. Population genomics of domestic and wild yeasts. Nature 458, 337–341 (2009). https://doi.org/10.1038/nature07743

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