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Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae

Nature volume 458, pages 342–345 (2009)Cite this article

Abstract

Comprehensive identification of polymorphisms among individuals within a species is essential both for studying the genetic basis of phenotypic differences and for elucidating the evolutionary history of the species. Large-scale polymorphism surveys have recently been reported for human1, mouse2 and Arabidopsis thaliana3. Here we report a nucleotide-level survey of genomic variation in a diverse collection of 63 Saccharomyces cerevisiae strains sampled from different ecological niches (beer, bread, vineyards, immunocompromised individuals, various fermentations and nature) and from locations on different continents. We hybridized genomic DNA from each strain to whole-genome tiling microarrays and detected 1.89 million single nucleotide polymorphisms, which were grouped into 101,343 distinct segregating sites. We also identified 3,985 deletion events of length >200 base pairs among the surveyed strains. We analysed the genome-wide patterns of nucleotide polymorphism and deletion variants, and measured the extent of linkage disequilibrium in S. cerevisiae. These results and the polymorphism resource we have generated lay the foundation for genome-wide association studies in yeast. We also examined the population structure of S. cerevisiae, providing support for multiple domestication events as well as insight into the origins of pathogenic strains.

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Figure 1: Decay of linkage disequilibrium as a function of distance.
Figure 2: Neighbour-joining tree of 63 S. cerevisiae strains.
Figure 3: Population structure of 63 S. cerevisiae strains.

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References

  1. The International HapMap Consortium. A haplotype map of the human genome. Nature 437, 1299–1320 (2005)

  2. Frazer, K. A. et al. A sequence-based variation map of 8.27 million SNPs in inbred mouse strains. Nature 448, 1050–1053 (2007)

    Article  ADS  CAS  Google Scholar 

  3. Clark, R. M. et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342 (2007)

    Article  ADS  CAS  Google Scholar 

  4. Kellis, M., Patterson, N., Endrizzi, M., Birren, B. & Lander, E. S. Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423, 241–254 (2003)

    Article  ADS  CAS  Google Scholar 

  5. Cliften, P. et al. Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301, 71–76 (2003)

    Article  ADS  CAS  Google Scholar 

  6. Dujon, B. et al. Genome evolution in yeasts. Nature 430, 35–44 (2004)

    Article  ADS  Google Scholar 

  7. Dujon, B. Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet. 22, 375–387 (2006)

    Article  CAS  Google Scholar 

  8. Gresham, D. et al. Genome-wide detection of polymorphisms at nucleotide resolution with a single DNA microarray. Science 311, 1932–1936 (2006)

    Article  ADS  CAS  Google Scholar 

  9. Carter, D. M. et al. Population genomics of domestic and wild yeasts. Nature (submitted)

  10. Gerton, J. L. et al. Inaugural article: global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 97, 11383–11390 (2000)

    Article  ADS  CAS  Google Scholar 

  11. Pryde, F. E., Gorham, H. C. & Louis, E. J. Chromosome ends: all the same under their caps. Curr. Opin. Genet. Dev. 7, 822–828 (1997)

    Article  CAS  Google Scholar 

  12. Schacherer, J. et al. Genome-wide analysis of nucleotide-level variation in commonly used Saccharomyces cerevisiae strains. PLoS ONE 2, e322 (2007)

    Article  ADS  Google Scholar 

  13. Winzeler, E. A. et al. Genetic diversity in yeast assessed with whole-genome oligonucleotide arrays. Genetics 163, 79–89 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901–906 (1999)

    Article  CAS  Google Scholar 

  15. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Fay, J. C. & Benavides, J. A. Evidence for domesticated and wild populations of Saccharomyces cerevisiae. PLoS Genet. 1, 66–71 (2005)

    Article  CAS  Google Scholar 

  17. Mortimer, R. K. & Johnston, J. R. Genealogy of principal strains of the yeast genetic stock center. Genetics 113, 35–43 (1986)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Enache-Angoulvant, A. & Hennequin, C. Invasive Saccharomyces infection: a comprehensive review. Clin. Infect. Dis. 41, 1559–1568 (2005)

    Article  Google Scholar 

  19. de Llanos, R., Querol, A., Peman, J., Gobernado, M. & Fernandez-Espinar, M. T. Food and probiotic strains from the Saccharomyces cerevisiae species as a possible origin of human systemic infections. Int. J. Food Microbiol. 110, 286–290 (2006)

    Article  CAS  Google Scholar 

  20. Steinmetz, L. M. et al. Dissecting the architecture of a quantitative trait locus in yeast. Nature 416, 326–330 (2002)

    Article  ADS  CAS  Google Scholar 

  21. Deutschbauer, A. M. & Davis, R. W. Quantitative trait loci mapped to single-nucleotide resolution in yeast. Nature Genet. 37, 1333–1340 (2005)

    Article  CAS  Google Scholar 

  22. Gatbonton, T. et al. Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet. 2, e35 (2006)

    Article  Google Scholar 

  23. Brem, R. B., Yvert, G., Clinton, R. & Kruglyak, L. Genetic dissection of transcriptional regulation in budding yeast. Science 296, 752–755 (2002)

    Article  ADS  CAS  Google Scholar 

  24. Perlstein, E. O., Ruderfer, D. M., Roberts, D. C., Schreiber, S. L. & Kruglyak, L. Genetic basis of individual differences in the response to small-molecule drugs in yeast. Nature Genet. 39, 496–502 (2007)

    Article  CAS  Google Scholar 

  25. Huson, D. H. & Bryant, D. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267 (2006)

    Article  CAS  Google Scholar 

  26. Thornton, K. Libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19, 2325–2327 (2003)

    Article  CAS  Google Scholar 

  27. Marjoram, P. & Wall, J. D. Fast “coalescent” simulation. BMC Genet. 7, 16 (2006)

    Article  Google Scholar 

  28. Fu, Y. X. Estimating effective population size or mutation rate using the frequencies of mutations of various classes in a sample of DNA sequences. Genetics 138, 1375–1386 (1994)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997)

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to all the researchers and institutions, and especially J. Fay, for sharing yeast strains. We thank K. Dolinski and J. Matese for technical support and D. Gresham for comments on the manuscript. The authors acknowledge discussions with members of the Kruglyak and Botstein laboratories. This work was supported by NIH grant R37 MH059520 and a James S. McDonnell Foundation Centennial Fellowship to L.K., and NIH grant GM071508 to the Lewis-Sigler Institute.

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Author notes

  1. Joseph Schacherer

    Present address: Present address: Department of Molecular Genetics, Genomics and Microbiology, Louis-Pasteur University and CNRS, UMR7156, Strasbourg 67083, France.,

  2. Joseph Schacherer and Joshua A. Shapiro: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology and Howard Hughes Medical Institute, Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA,

    Joseph Schacherer, Joshua A. Shapiro, Douglas M. Ruderfer & Leonid Kruglyak

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  1. Joseph Schacherer
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  4. Leonid Kruglyak
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Corresponding author

Correspondence to Leonid Kruglyak.

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Schacherer, J., Shapiro, J., Ruderfer, D. et al. Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae. Nature 458, 342–345 (2009). https://doi.org/10.1038/nature07670

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