Fog signaling has diverse roles in epithelial morphogenesis in insects

Author:

Benton Matthew Alan12ORCID,Frey Nadine1,Nunes da Fonseca Rodrigo1,von Levetzow Cornelia1,Stappert Dominik1,Hakeemi Muhammad Salim1,Conrads Kai H1,Pechmann Matthias1ORCID,Panfilio Kristen A13ORCID,Lynch Jeremy A4ORCID,Roth Siegfried1ORCID

Affiliation:

1. Institute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, Germany

2. Department of Zoology, University of Cambridge, Cambridge, United Kingdom

3. School of Life Sciences, University of Warwick, Coventry, United Kingdom

4. Department of Biological Sciences, University of Illinois, Chicago, United States

Abstract

The Drosophila Fog pathway represents one of the best-understood signaling cascades controlling epithelial morphogenesis. During gastrulation, Fog induces apical cell constrictions that drive the invagination of mesoderm and posterior gut primordia. The cellular mechanisms underlying primordia internalization vary greatly among insects and recent work has suggested that Fog signaling is specific to the fast mode of gastrulation found in some flies. On the contrary, here we show in the beetle Tribolium, whose development is broadly representative for insects, that Fog has multiple morphogenetic functions. It modulates mesoderm internalization and controls a massive posterior infolding involved in gut and extraembryonic development. In addition, Fog signaling affects blastoderm cellularization, primordial germ cell positioning, and cuboidal-to-squamous cell shape transitions in the extraembryonic serosa. Comparative analyses with two other distantly related insect species reveals that Fog’s role during cellularization is widely conserved and therefore might represent the ancestral function of the pathway.

Funder

Deutsche Forschungsgemeinschaft

University of Cologne

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Boehringer Ingelheim Fonds

National Institutes of Health

Alexander von Humboldt Foundation

Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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