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Assessing the complex architecture of polygenic traits in diverged yeast populations

Authors

  • FRANCISCO A. CUBILLOS,

    1. Centre for Genetics and Genomics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK
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  • ELEONORA BILLI,

    1. Centre for Genetics and Genomics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK
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    • Present address: (E.B.), Department for Molecular Biomedical Research, VIB and Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium. (P.F.) CNRS UMR6247, Génétique, Réproduction et Développement (GReD), Clermont Université, 24 avenue des Landais, 63177 Aubière Cedex, France.

  • ENIKÖ ZÖRGÖ,

    1. Department of Cell and Molecular Biology, University of Gothenburg, 41390 Gothenburg, Sweden
    2. Centre for Integrative Genetics (CIGENE), Norwegian University of Life Sciences (UMB), PO Box 5003, 1432 Ås, Norway
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  • LEOPOLD PARTS,

    1. The Wellcome Trust Sanger Institute, Hinxton, CB10 1SA, UK
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  • PATRICK FARGIER,

    1. Centre for Genetics and Genomics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK
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    • Present address: (E.B.), Department for Molecular Biomedical Research, VIB and Department of Biomedical Molecular Biology, Ghent University, Ghent, Belgium. (P.F.) CNRS UMR6247, Génétique, Réproduction et Développement (GReD), Clermont Université, 24 avenue des Landais, 63177 Aubière Cedex, France.

  • STIG OMHOLT,

    1. Centre for Integrative Genetics (CIGENE), Norwegian University of Life Sciences (UMB), PO Box 5003, 1432 Ås, Norway
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  • ANDERS BLOMBERG,

    1. Department of Cell and Molecular Biology, University of Gothenburg, 41390 Gothenburg, Sweden
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  • JONAS WARRINGER,

    1. Department of Cell and Molecular Biology, University of Gothenburg, 41390 Gothenburg, Sweden
    2. Centre for Integrative Genetics (CIGENE), Norwegian University of Life Sciences (UMB), PO Box 5003, 1432 Ås, Norway
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  • EDWARD J. LOUIS,

    1. Centre for Genetics and Genomics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK
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    • These authors contributed equally to this work.

  • GIANNI LITI

    1. Centre for Genetics and Genomics, Queen’s Medical Centre, University of Nottingham, Nottingham, NG7 2UH, UK
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    • These authors contributed equally to this work.


Gianni Liti or Edward J. Louis, Fax: +44 115 8231140; E-mail: gianni.liti@nottingham.ac.uk or ed.louis@nottingham.ac.uk.

Abstract

Phenotypic variation arising from populations adapting to different niches has a complex underlying genetic architecture. A major challenge in modern biology is to identify the causative variants driving phenotypic variation. Recently, the baker’s yeast, Saccharomyces cerevisiae has emerged as a powerful model for dissecting complex traits. However, past studies using a laboratory strain were unable to reveal the complete architecture of polygenic traits. Here, we present a linkage study using 576 recombinant strains obtained from crosses of isolates representative of the major lineages. The meiotic recombinational landscape appears largely conserved between populations; however, strain-specific hotspots were also detected. Quantitative measurements of growth in 23 distinct ecologically relevant environments show that our recombinant population recapitulates most of the standing phenotypic variation described in the species. Linkage analysis detected an average of 6.3 distinct QTLs for each condition tested in all crosses, explaining on average 39% of the phenotypic variation. The QTLs detected are not constrained to a small number of loci, and the majority are specific to a single cross-combination and to a specific environment. Moreover, crosses between strains of similar phenotypes generate greater variation in the offspring, suggesting the presence of many antagonistic alleles and epistatic interactions. We found that subtelomeric regions play a key role in defining individual quantitative variation, emphasizing the importance of the adaptive nature of these regions in natural populations. This set of recombinant strains is a powerful tool for investigating the complex architecture of polygenic traits.

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