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Research Article

Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae

Paul M. Magwene, Ömür Kayıkçı, Joshua A. Granek, Jennifer M. Reininga, Zackary Scholl, and Debra Murray
  1. Department of Biology and Institute for Genome Sciences and Policy Center for Systems Biology, Duke University, Durham, NC 27708

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PNAS February 1, 2011 108 (5) 1987-1992; https://doi.org/10.1073/pnas.1012544108
Paul M. Magwene
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  • For correspondence: paul.magwene@duke.edu
Ömür Kayıkçı
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Joshua A. Granek
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Jennifer M. Reininga
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Zackary Scholl
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Debra Murray
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  1. Edited* by Sean B. Carroll, University of Wisconsin, Madison, WI, and approved December 16, 2010 (received for review August 23, 2010)

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Abstract

We carried out a population genomic survey of Saccharomyces cerevisiae diploid isolates and find that many budding yeast strains have high levels of genomic heterozygosity, much of which is likely due to outcrossing. We demonstrate that variation in heterozygosity among strains is correlated with a life-history trade-off that involves how readily yeast switch from asexual to sexual reproduction under nutrient stress. This trade-off is reflected in a negative relationship between sporulation efficiency and pseudohyphal development and correlates with variation in the expression of RME1, a transcription factor with pleiotropic effects on meiosis and filamentous growth. Selection for alternate life-history strategies in natural versus human-associated environments likely contributes to differential maintenance of genomic heterozygosity through its effect on the frequency that yeast lineages experience sexual cycles and hence the opportunity for inbreeding. In addition to elevated levels of heterozygosity, many strains exhibit large genomic regions of loss-of-heterozygosity (LOH), suggesting that mitotic recombination has a significant impact on genetic variation in this species. This study provides new insights into the roles that both outcrossing and mitotic recombination play in shaping the genome architecture of Saccharomyces cerevisiae. This study also provides a unique case where stark differences in the genomic distribution of genetic variation among individuals of the same species can be largely explained by a life-history trade-off.

Footnotes

  • 1To whom correspondence should be addressed. E-mail: paul.magwene{at}duke.edu.
  • Author contributions: P.M.M. designed research; P.M.M., Ö.K., J.A.G., J.M.R., and D.M. performed research; P.M.M., Ö.K., J.A.G., and Z.S. analyzed data; and P.M.M., J.M.R., and D.M. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • Data deposition: The sequences reported in this paper have been deposited in the National Institutes of Health Short Read Archive (accession nos. SRX030121–SRX030126, SRX030131– SRX030135, and SRX030579).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1012544108/-/DCSupplemental.

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Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae
Paul M. Magwene, Ömür Kayıkçı, Joshua A. Granek, Jennifer M. Reininga, Zackary Scholl, Debra Murray
Proceedings of the National Academy of Sciences Feb 2011, 108 (5) 1987-1992; DOI: 10.1073/pnas.1012544108

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Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae
Paul M. Magwene, Ömür Kayıkçı, Joshua A. Granek, Jennifer M. Reininga, Zackary Scholl, Debra Murray
Proceedings of the National Academy of Sciences Feb 2011, 108 (5) 1987-1992; DOI: 10.1073/pnas.1012544108
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Proceedings of the National Academy of Sciences: 108 (5)
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