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.
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
Further reading
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- Cell Biology
- Developmental Biology
Eukaryotic cells depend on exocytosis to direct intracellularly synthesized material toward the extracellular space or the plasma membrane, so exocytosis constitutes a basic function for cellular homeostasis and communication between cells. The secretory pathway includes biogenesis of secretory granules (SGs), their maturation and fusion with the plasma membrane (exocytosis), resulting in release of SG content to the extracellular space. The larval salivary gland of Drosophila melanogaster is an excellent model for studying exocytosis. This gland synthesizes mucins that are packaged in SGs that sprout from the trans-Golgi network and then undergo a maturation process that involves homotypic fusion, condensation, and acidification. Finally, mature SGs are directed to the apical domain of the plasma membrane with which they fuse, releasing their content into the gland lumen. The exocyst is a hetero-octameric complex that participates in tethering of vesicles to the plasma membrane during constitutive exocytosis. By precise temperature-dependent gradual activation of the Gal4-UAS expression system, we have induced different levels of silencing of exocyst complex subunits, and identified three temporarily distinctive steps of the regulated exocytic pathway where the exocyst is critically required: SG biogenesis, SG maturation, and SG exocytosis. Our results shed light on previously unidentified functions of the exocyst along the exocytic pathway. We propose that the exocyst acts as a general tethering factor in various steps of this cellular process.
