1. Cell Biology
  2. Evolutionary Biology
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A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization

  1. Omaya Dudin  Is a corresponding author
  2. Andrej Ondracka
  3. Xavier Grau-Bové
  4. Arthur AB Haraldsen
  5. Atsushi Toyoda
  6. Hiroshi Suga
  7. Jon Bråte
  8. Iñaki Ruiz-Trillo  Is a corresponding author
  1. CSIC-Universitat Pompeu Fabra, Spain
  2. University of Oslo, Norway
  3. National Institute of Genetics, Japan
  4. Prefectural University of Hiroshima, Japan
Research Article
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Cite this article as: eLife 2019;8:e49801 doi: 10.7554/eLife.49801

Abstract

In animals, cellularization of a coenocyte is a specialized form of cytokinesis that results in the formation of a polarized epithelium during early embryonic development. It is characterized by coordinated assembly of an actomyosin network, which drives inward membrane invaginations. However, whether coordinated cellularization driven by membrane invagination exists outside animals is not known. To that end, we investigate cellularization in the ichthyosporean Sphaeroforma arctica, a close unicellular relative of animals. We show that the process of cellularization involves coordinated inward plasma membrane invaginations dependent on an actomyosin network and reveal the temporal order of its assembly. This leads to the formation of a polarized layer of cells resembling an epithelium. We show that this stage is associated with tightly regulated transcriptional activation of genes involved in cell adhesion. Hereby we demonstrate the presence of a self-organized, clonally-generated, polarized layer of cells in a unicellular relative of animals.

Data availability

Sequencing data have been deposited at the following locations :S. arctica genome assembly - BioProject number PRJDB8476S. arctica transcriptomes - PRJEB32922 (ERP115662) on European Nucleotide Archive

The following data sets were generated

Article and author information

Author details

  1. Omaya Dudin

    Institut de Biologia Evolutiva, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
    For correspondence
    omaya.dudin@outlook.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6673-3149
  2. Andrej Ondracka

    Institut de Biologia Evolutiva, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Xavier Grau-Bové

    Institut de Biologia Evolutiva, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
    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
  4. Arthur AB Haraldsen

    Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  5. Atsushi Toyoda

    Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0728-7548
  6. Hiroshi Suga

    Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Shobara, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Jon Bråte

    Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0490-1175
  8. Iñaki Ruiz-Trillo

    Institut de Biologia Evolutiva, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
    For correspondence
    inaki.ruiz@ibe.upf-csic.es
    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

European Research Council Consolidator Grant (ERC-2012-Co -616960)

  • Iñaki Ruiz-Trillo

MEXT KAKENHI (221S0002)

  • Atsushi Toyoda

MEXT KAKENHI (26891021)

  • Hiroshi Suga

Young Research Talents grant from the Research Council of Norway (240284)

  • Jon Bråte

Swiss National Science Foundation (P2LAP3_171815)

  • Omaya Dudin

Marie Sklodowska-Curie individual fellowship (MSCA-IF 746044)

  • Omaya Dudin

Marie Sklodowska-Curie individual fellowship (MSCA-IF 747086)

  • Andrej Ondracka

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

Reviewing Editor

  1. Mukund Thattai, National Centre for Biological Sciences, India

Publication history

  1. Received: June 29, 2019
  2. Accepted: October 23, 2019
  3. Accepted Manuscript published: October 24, 2019 (version 1)
  4. Accepted Manuscript updated: October 28, 2019 (version 2)
  5. Version of Record published: November 14, 2019 (version 3)
  6. Version of Record updated: June 19, 2020 (version 4)

Copyright

© 2019, Dudin 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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Further reading

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