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Elife. 2019 Oct 28;8. pii: e49801. doi: 10.7554/eLife.49801.

A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization.

Author information

1
Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain.
2
Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
3
Section for Genetics and Evolutionary Biology (EVOGENE), Department of Biosciences, University of Oslo, Oslo, Norway.
4
Department of Genomics and Evolutionary Biology, National Institute of Genetics, Mishima, Japan.
5
Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Hiroshima, Japan.
6
Departament de Genètica, Microbiologia i Estadística, Universitat de Barcelona, Barcelona, Spain.
7
ICREA, Barcelona, Spain.
#
Contributed equally

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.

KEYWORDS:

actin; cell biology; cellularization; coenocyte; epithelium; evolution; evolutionary biology; multicellularity

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