Fog signaling has diverse roles in epithelial morphogenesis in insects
- University of Cologne, Germany
- University of Illinois at 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 cellularisation is widely conserved and therefore might represent the ancestral function of the pathway.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. The Supplemental Material File 1 contains all primers used to amplify sequences for production of antisense RNA (ISH) and dsRNA (RNAi).
Article and author information
Author details
Matthew Alan Benton
Kristen A Panfilio
Funding
Deutsche Forschungsgemeinschaft (CRC 680)
- Nadine Frey
Deutsche Forschungsgemeinschaft
- Kai H Conrads
University of Cologne (Postdoctoral grant)
- Matthias Pechmann
Deutsche Forschungsgemeinschaft (CRC 680)
- Siegfried Roth
Deutsche Forschungsgemeinschaft (DFG Research Fellowship 407643416)
- Matthew Alan Benton
FAPERJ
- Rodrigo Nunes da Fonseca
University of Cologne (International Graduate School in Genetics and Functional Genomics)
- Rodrigo Nunes da Fonseca
- Cornelia von Levetzow
CNPq
- Rodrigo Nunes da Fonseca
CAPES
- Rodrigo Nunes da Fonseca
Deutsche Forschungsgemeinschaft (RU 1234)
- Muhammad Salim Hakeemi
Boehringer Ingelheim Fonds (PhD fellowship)
- Dominik Stappert
Deutsche Forschungsgemeinschaft (Emmy Noether Program PA 2044/1-1))
- Kristen A Panfilio
National Institutes of Health (R03 HD078578)
- Jeremy A Lynch
Alexander von Humboldt Foundation (Postdoctoral Felloship)
- Matthew Alan Benton
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India
Version history
- Received: April 2, 2019
- Accepted: September 30, 2019
- Accepted Manuscript published: October 1, 2019 (version 1)
- Version of Record published: October 15, 2019 (version 2)
Copyright
© 2019, Benton 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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Fog signaling has diverse roles in epithelial morphogenesis in insects
eLife 8:e47346.
https://doi.org/10.7554/eLife.47346
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