A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization
- CSIC-Universitat Pompeu Fabra, Spain
- University of Oslo, Norway
- National Institute of Genetics, Japan
- Prefectural University of Hiroshima, Japan
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
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Sphaeroforma arctica genome assemblyNCBI BioProject, PRJDB8476.
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Dynamics of transcription during the coenocytic cycle of Sphaeroforma arcticaEuropean nucleotide archive, PRJEB32922 (ERP115662).
Article and author information
Author details
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
- Mukund Thattai, National Centre for Biological Sciences, India
Version history
- Received: June 29, 2019
- Accepted: October 23, 2019
- Accepted Manuscript published: October 24, 2019 (version 1)
- Accepted Manuscript updated: October 28, 2019 (version 2)
- Version of Record published: November 14, 2019 (version 3)
- 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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A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization
eLife 8:e49801.
https://doi.org/10.7554/eLife.49801
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