Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals

  1. Alex de Mendoza  Is a corresponding author
  2. Hiroshi Suga
  3. Jon Permanyer
  4. Manuel Irimia
  5. Iñaki Ruiz-Trillo
  1. The University of Western Australia, Australia
  2. Universitat Pompeu Fabra, Spain
  3. Centre for Genomic Regulation, Spain

Abstract

Cell-type specification through differential genome regulation is a hallmark of complex multicellularity. However, it remains unclear how this process evolved during the transition from unicellular to multicellular organisms. To address this question, we investigated transcriptional dynamics in the ichthyosporean Creolimax fragrantissima, a relative of animals that undergoes coenocytic development. We find that Creolimax utilizes dynamic regulation of alternative splicing, long inter-genic non-coding RNAs and co-regulated gene modules associated with animal multicellularity in a cell-type specific manner. Moreover, our study suggests that the different cell types of the three closest animal relatives (ichthyosporeans, filastereans and choanoflagellates) are the product of lineage-specific innovations. Additionally, a proteomic survey of the secretome reveals adaptations to a fungal-like lifestyle. In summary, the diversity of cell types among protistan relatives of animals and their complex genome regulation demonstrates that the last unicellular ancestor of animals was already capable of elaborate specification of cell types.

Article and author information

Author details

  1. Alex de Mendoza

    ARC CoE Plant Energy Biology, The University of Western Australia, Crawley, Australia
    For correspondence
    alexmendozasoler@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Hiroshi Suga

    Institut de Biologia Evolutiva, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Jon Permanyer

    EMBL-CRG Systems Biology Unit, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Manuel Irimia

    EMBL-CRG Systems Biology Unit, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Iñaki Ruiz-Trillo

    Institut de Biologia Evolutiva, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States

Publication history

  1. Received: May 21, 2015
  2. Accepted: October 13, 2015
  3. Accepted Manuscript published: October 14, 2015 (version 1)
  4. Version of Record published: January 21, 2016 (version 2)

Copyright

© 2015, de Mendoza 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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  1. Alex de Mendoza
  2. Hiroshi Suga
  3. Jon Permanyer
  4. Manuel Irimia
  5. Iñaki Ruiz-Trillo
(2015)
Complex transcriptional regulation and independent evolution of fungal-like traits in a relative of animals
eLife 4:e08904.
https://doi.org/10.7554/eLife.08904

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