1. Chromosomes and Gene Expression
  2. Genetics and Genomics
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Dynamics of genomic innovation in the unicellular ancestry of animals

  1. Xavier Grau-Bové  Is a corresponding author
  2. Guifré Torruella
  3. Stuart Donachie
  4. Hiroshi Suga
  5. Guy Leonard
  6. Thomas A Richards
  7. Iñaki Ruiz-Trillo  Is a corresponding author
  1. Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Spain
  2. Université Paris-Sud/Paris-Saclay, France
  3. University of Hawai'i at Mānoa, United States
  4. Prefectural University of Hiroshima, Japan
  5. Living Systems Institute, United Kingdom
  6. University of Exeter, United Kingdom
Research Article
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Cite this article as: eLife 2017;6:e26036 doi: 10.7554/eLife.26036

Abstract

Which genomic innovations underpinned the origin of multicellular animals is still an open debate. Here, we investigate this question by reconstructing the genome architecture and gene family diversity of ancestral premetazoans, aiming to date the emergence of animal-like traits. Our comparative analysis involves genomes from animals and their closest unicellular relatives (the Holozoa), including four new genomes: three Ichthyosporea and Corallochytrium limacisporum. Here we show that the earliest animals were shaped by dynamic changes in genome architecture before the emergence of multicellularity: an early burst of gene diversity in the ancestor of Holozoa, enriched in transcription factors and cell adhesion machinery, was followed by multiple and differently-timed episodes of synteny disruption, intron gain and genome expansions. Thus, the foundations of animal genome architecture were laid before the origin of complex multicellularity – highlighting the necessity of a unicellular perspective to understand early animal evolution.

Article and author information

Author details

  1. Xavier Grau-Bové

    Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
    For correspondence
    xavier.graubove@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1978-5824
  2. Guifré Torruella

    Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, Orsay, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6534-4758
  3. Stuart Donachie

    Department of Microbiology, University of Hawai'i at Mānoa, Honolulu, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Hiroshi Suga

    Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Shobara, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Guy Leonard

    Department of Biosciences, Living Systems Institute, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4607-2064
  6. Thomas A Richards

    Department of Biosciences, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Iñaki Ruiz-Trillo

    Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain
    For correspondence
    inaki.ruiz@multicellgenome.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6547-5304

Funding

Ministerio de Economía y Competitividad (BFU2014-57779-P)

  • Iñaki Ruiz-Trillo

European Commission (ERC-2012-Co -616960)

  • Iñaki Ruiz-Trillo

Ministerio de Economía y Competitividad (BFU-2011-23434)

  • Iñaki Ruiz-Trillo

Generalitat de Catalunya (2014 SGR 619)

  • Iñaki Ruiz-Trillo

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Diethard Tautz, Max-Planck Institute for Evolutionary Biology, Germany

Publication history

  1. Received: February 21, 2017
  2. Accepted: July 11, 2017
  3. Accepted Manuscript published: July 20, 2017 (version 1)
  4. Version of Record published: August 17, 2017 (version 2)
  5. Version of Record updated: March 1, 2018 (version 3)

Copyright

© 2017, Grau-Bové et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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