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A Unicellular Relative of Animals Generates an Epithelium-Like Cell Layer by Actomyosin-dependent Cellularization

58 Pages Posted: 1 Apr 2019 Publication Status: Review Complete

See all articles by Omaya Dudin

Omaya Dudin

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Andrej Ondracka

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Xavier Grau-Bove

Universitat Pompeu Fabra - Institute of Evolutionary Biology; Liverpool School of Tropical Medicine - Vector Biology Department

Arthur A. B. Haraldsen

University of Oslo - Section for Genetics and Evolutionary Biology (EVOGENE)

Atsushi Toyoda

National Institute of Genetics - Department of Genomics and Evolutionary Biology

Hiroshi Suga

Prefectural University of Hiroshima - Faculty of Life and Environmental Sciences

Jon Brate

University of Oslo - Section for Genetics and Evolutionary Biology (EVOGENE)

Inaki Ruiz-Trillo

Universitat Pompeu Fabra - Institute of Evolutionary Biology; University of Barcelona - Department of Genetics; ICREA

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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 epithelium-like stage is associated with tightly regulated transcriptional activation of genes involved in cell adhesion. Hereby we demonstrate the presence of a selforganized, clonally-generated, polarized layer of cells in a unicellular relative of animals.

Keywords: Cellularization, Coenocyte, Evolution, Epithelium, Actin, Multicellularity, Ichthyosporea

Suggested Citation

Dudin, Omaya and Ondracka, Andrej and Grau-Bove, Xavier and Haraldsen, Arthur A. B. and Toyoda, Atsushi and Suga, Hiroshi and Brate, Jon and Ruiz-Trillo, Inaki, A Unicellular Relative of Animals Generates an Epithelium-Like Cell Layer by Actomyosin-dependent Cellularization (March 29, 2019). Available at SSRN: https://ssrn.com/abstract=3362312 or http://dx.doi.org/10.2139/ssrn.3362312
This version of the paper has not been formally peer reviewed.

Omaya Dudin

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Ramon Trias Fargas, 25-27
Barcelona, E-08005
Spain

Andrej Ondracka

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Ramon Trias Fargas, 25-27
Barcelona, E-08005
Spain

Xavier Grau-Bove

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Ramon Trias Fargas, 25-27
Barcelona, E-08005
Spain

Liverpool School of Tropical Medicine - Vector Biology Department

Liverpool
United Kingdom

Arthur A. B. Haraldsen

University of Oslo - Section for Genetics and Evolutionary Biology (EVOGENE)

PO Box 6706 St Olavs plass
Oslo, N-0317
Norway

Atsushi Toyoda

National Institute of Genetics - Department of Genomics and Evolutionary Biology

Yata 1111
Mishima
Shizuoka 411-8540
Japan

Hiroshi Suga

Prefectural University of Hiroshima - Faculty of Life and Environmental Sciences

Nanatsuka 5562
Hiroshima 727-0023
Japan

Jon Brate

University of Oslo - Section for Genetics and Evolutionary Biology (EVOGENE)

PO Box 6706 St Olavs plass
Oslo, N-0317
Norway

Inaki Ruiz-Trillo (Contact Author)

Universitat Pompeu Fabra - Institute of Evolutionary Biology ( email )

Ramon Trias Fargas, 25-27
Barcelona, E-08005
Spain

University of Barcelona - Department of Genetics ( email )

Barcelona, 08028
Spain

ICREA ( email )

P/ Lluis Companys 23
Barcelona, 08010
Spain