Fog signaling has diverse roles in epithelial morphogenesis in insects.

Matthew Alan Benton,Nadine Frey,Siegfried Roth,Matthias Pechmann,Kristen A Panfilio,Dominik Stappert,Kai H Conrads,Muhammad Salim Hakeemi,Jeremy A Lynch,Cornelia Von Levetzow,Rodrigo Nunes Da Fonseca

doi:10.7554/elife.47346

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.

Highlights

The Folded gastrulation (Fog) pathway is one of the few signaling pathways dedicated to epithelial morphogenesis (Gilmour et al, 2017; Manning and Rogers, 2014)
Fog signaling was discovered in the fly Drosophila melanogaster, where it is required for the formation of two major epithelial folds during early embryogenesis: the ventral furrow, and the posterior gut fold (Costa et al, 1994; Parks and Wieschaus, 1991; Sweeton et al, 1991; Zusman and Wieschaus, 1985)
In this article we have shown that Fog signaling plays major morphogenetic roles during embryogenesis in the beetle Tribolium (Figures 3 and 11)

Summary

Introduction

The Folded gastrulation (Fog) pathway is one of the few signaling pathways dedicated to epithelial morphogenesis (Gilmour et al, 2017; Manning and Rogers, 2014). Fog itself is an extracellular ligand that is secreted by future invaginating cells (Dawes-Hoang et al, 2005) and activates two G protein-coupled receptors (GPCRs): Mist (Mesoderm-invagination signal transducer, known as Mthl1 [Methuselah-like1]) (Manning et al, 2013) and Smog (Jha et al, 2018; Kerridge et al, 2016). Activation of these receptors causes Concertina (Cta), the Ga12/13 subunit of a trimeric G protein, to recruit RhoGEF2 to the apical plasma membrane, where it Benton et al eLife 2019;8:e47346.

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Conclusion