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Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

Author

Listed:
  • David Peris

    (University of Wisconsin-Madison
    University of Wisconsin-Madison
    University of Oslo
    Institute of Agrochemistry and Food Technology (IATA), CSIC)

  • Emily J. Ubbelohde

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Meihua Christina Kuang

    (University of Wisconsin-Madison)

  • Jacek Kominek

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Quinn K. Langdon

    (University of Wisconsin-Madison)

  • Marie Adams

    (Biotechnology Center, University of Wisconsin-Madison)

  • Justin A. Koshalek

    (Biotechnology Center, University of Wisconsin-Madison)

  • Amanda Beth Hulfachor

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Dana A. Opulente

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • David J. Hall

    (University of Utrecht)

  • Katie Hyma

    (University of Rochester)

  • Justin C. Fay

    (University of Rochester)

  • Jean-Baptiste Leducq

    (Université de Montréal
    Université Laval)

  • Guillaume Charron

    (Laurentian Forestry Centre)

  • Christian R. Landry

    (Université Laval)

  • Diego Libkind

    (Científicas y Técnicas (CONICET)-Universidad Nacional del Comahue)

  • Carla Gonçalves

    (University of Wisconsin-Madison
    Universidade NOVA de Lisboa
    Universidade Nova de Lisboa
    Vanderbilt University, Department of Biological Sciences)

  • Paula Gonçalves

    (Universidade Nova de Lisboa)

  • José Paulo Sampaio

    (Universidade Nova de Lisboa)

  • Qi-Ming Wang

    (University of Wisconsin-Madison
    Hebei University)

  • Feng-Yan Bai

    (Chinese Academy of Sciences)

  • Russel L. Wrobel

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

  • Chris Todd Hittinger

    (University of Wisconsin-Madison
    University of Wisconsin-Madison)

Abstract

Species is the fundamental unit to quantify biodiversity. In recent years, the model yeast Saccharomyces cerevisiae has seen an increased number of studies related to its geographical distribution, population structure, and phenotypic diversity. However, seven additional species from the same genus have been less thoroughly studied, which has limited our understanding of the macroevolutionary events leading to the diversification of this genus over the last 20 million years. Here, we show the geographies, hosts, substrates, and phylogenetic relationships for approximately 1,800 Saccharomyces strains, covering the complete genus with unprecedented breadth and depth. We generated and analyzed complete genome sequences of 163 strains and phenotyped 128 phylogenetically diverse strains. This dataset provides insights about genetic and phenotypic diversity within and between species and populations, quantifies reticulation and incomplete lineage sorting, and demonstrates how gene flow and selection have affected traits, such as galactose metabolism. These findings elevate the genus Saccharomyces as a model to understand biodiversity and evolution in microbial eukaryotes.

Suggested Citation

  • David Peris & Emily J. Ubbelohde & Meihua Christina Kuang & Jacek Kominek & Quinn K. Langdon & Marie Adams & Justin A. Koshalek & Amanda Beth Hulfachor & Dana A. Opulente & David J. Hall & Katie Hyma , 2023. "Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36139-2
    DOI: 10.1038/s41467-023-36139-2
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    References listed on IDEAS

    as
    1. G. Fischer & S. A. James & I. N. Roberts & S. G. Oliver & E. J. Louis, 2000. "Chromosomal evolution in Saccharomyces," Nature, Nature, vol. 405(6785), pages 451-454, May.
    2. Shou-Fu Duan & Pei-Jie Han & Qi-Ming Wang & Wan-Qiu Liu & Jun-Yan Shi & Kuan Li & Xiao-Ling Zhang & Feng-Yan Bai, 2018. "The origin and adaptive evolution of domesticated populations of yeast from Far East Asia," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Jackson Peter & Matteo De Chiara & Anne Friedrich & Jia-Xing Yue & David Pflieger & Anders Bergström & Anastasie Sigwalt & Benjamin Barre & Kelle Freel & Agnès Llored & Corinne Cruaud & Karine Labadie, 2018. "Genome evolution across 1,011 Saccharomyces cerevisiae isolates," Nature, Nature, vol. 556(7701), pages 339-344, April.
    4. Pedro Almeida & Carla Gonçalves & Sara Teixeira & Diego Libkind & Martin Bontrager & Isabelle Masneuf-Pomarède & Warren Albertin & Pascal Durrens & David James Sherman & Philippe Marullo & Chris Todd , 2014. "A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum," Nature Communications, Nature, vol. 5(1), pages 1-12, September.
    5. Marcell K. Peters & Andreas Hemp & Tim Appelhans & Christina Behler & Alice Classen & Florian Detsch & Andreas Ensslin & Stefan W. Ferger & Sara B. Frederiksen & Friederike Gebert & Michael Haas & Mar, 2016. "Predictors of elevational biodiversity gradients change from single taxa to the multi-taxa community level," Nature Communications, Nature, vol. 7(1), pages 1-11, December.
    6. Daniela Delneri & Isabelle Colson & Sofia Grammenoudi & Ian N. Roberts & Edward J. Louis & Stephen G. Oliver, 2003. "Engineering evolution to study speciation in yeasts," Nature, Nature, vol. 422(6927), pages 68-72, March.
    7. Jing Hou & Anne Friedrich & Jean-Sebastien Gounot & Joseph Schacherer, 2015. "Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast," Nature Communications, Nature, vol. 6(1), pages 1-8, November.
    8. Gianni Liti & David M. Carter & Alan M. Moses & Jonas Warringer & Leopold Parts & Stephen A. James & Robert P. Davey & Ian N. Roberts & Austin Burt & Vassiliki Koufopanou & Isheng J. Tsai & Casey M. B, 2009. "Population genomics of domestic and wild yeasts," Nature, Nature, vol. 458(7236), pages 337-341, March.
    9. Xing-Xing Shen & Yuanning Li & Chris Todd Hittinger & Xue-xin Chen & Antonis Rokas, 2020. "An investigation of irreproducibility in maximum likelihood phylogenetic inference," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    10. Daniel John Lawson & Garrett Hellenthal & Simon Myers & Daniel Falush, 2012. "Inference of Population Structure using Dense Haplotype Data," PLOS Genetics, Public Library of Science, vol. 8(1), pages 1-16, January.
    11. Chris Todd Hittinger & Paula Gonçalves & José Paulo Sampaio & Jim Dover & Mark Johnston & Antonis Rokas, 2010. "Remarkably ancient balanced polymorphisms in a multi-locus gene network," Nature, Nature, vol. 464(7285), pages 54-58, March.
    12. Antonis Rokas & Barry L. Williams & Nicole King & Sean B. Carroll, 2003. "Genome-scale approaches to resolving incongruence in molecular phylogenies," Nature, Nature, vol. 425(6960), pages 798-804, October.
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