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Powerful decomposition of complex traits in a diploid model

Author

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  • Johan Hallin

    (Institute for Research on Cancer and Aging, Nice (IRCAN), CNRS UMR7284, INSERM U1081, University of Nice Sophia Antipolis)

  • Kaspar Märtens

    (Institute of Computer Science, University of Tartu)

  • Alexander I. Young

    (Wellcome Trust Centre for Human Genetics, University of Oxford)

  • Martin Zackrisson

    (Gothenburg University)

  • Francisco Salinas

    (Institute for Research on Cancer and Aging, Nice (IRCAN), CNRS UMR7284, INSERM U1081, University of Nice Sophia Antipolis
    Present address: Millennium Nucleus for Fungal Integrative and Synthetic Biology (MN-FISB); Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Casilla 114-D, 8331150 Santiago, Chile)

  • Leopold Parts

    (Institute of Computer Science, University of Tartu
    Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus)

  • Jonas Warringer

    (Gothenburg University
    Centre for Integrative Genetics (CIGENE), Norwegian University of Life Sciences)

  • Gianni Liti

    (Institute for Research on Cancer and Aging, Nice (IRCAN), CNRS UMR7284, INSERM U1081, University of Nice Sophia Antipolis)

Abstract

Explaining trait differences between individuals is a core and challenging aim of life sciences. Here, we introduce a powerful framework for complete decomposition of trait variation into its underlying genetic causes in diploid model organisms. We sequence and systematically pair the recombinant gametes of two intercrossed natural genomes into an array of diploid hybrids with fully assembled and phased genomes, termed Phased Outbred Lines (POLs). We demonstrate the capacity of this approach by partitioning fitness traits of 6,642 Saccharomyces cerevisiae POLs across many environments, achieving near complete trait heritability and precisely estimating additive (73%), dominance (10%), second (7%) and third (1.7%) order epistasis components. We map quantitative trait loci (QTLs) and find nonadditive QTLs to outnumber (3:1) additive loci, dominant contributions to heterosis to outnumber overdominant, and extensive pleiotropy. The POL framework offers the most complete decomposition of diploid traits to date and can be adapted to most model organisms.

Suggested Citation

  • Johan Hallin & Kaspar Märtens & Alexander I. Young & Martin Zackrisson & Francisco Salinas & Leopold Parts & Jonas Warringer & Gianni Liti, 2016. "Powerful decomposition of complex traits in a diploid model," Nature Communications, Nature, vol. 7(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms13311
    DOI: 10.1038/ncomms13311
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    Cited by:

    1. Danesh Moradigaravand & Martin Palm & Anne Farewell & Ville Mustonen & Jonas Warringer & Leopold Parts, 2018. "Prediction of antibiotic resistance in Escherichia coli from large-scale pan-genome data," PLOS Computational Biology, Public Library of Science, vol. 14(12), pages 1-17, December.
    2. Takeshi Matsui & Martin N. Mullis & Kevin R. Roy & Joseph J. Hale & Rachel Schell & Sasha F. Levy & Ian M. Ehrenreich, 2022. "The interplay of additivity, dominance, and epistasis on fitness in a diploid yeast cross," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Simone Mozzachiodi & Lorenzo Tattini & Agnes Llored & Agurtzane Irizar & Neža Škofljanc & Melania D’Angiolo & Matteo De Chiara & Benjamin P. Barré & Jia-Xing Yue & Angela Lutazi & Sophie Loeillet & Ra, 2021. "Aborting meiosis allows recombination in sterile diploid yeast hybrids," Nature Communications, Nature, vol. 12(1), pages 1-13, December.

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