Fog signaling has diverse roles in epithelial morphogenesis in insects

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 inter...

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Main Authors: Matthew Alan Benton, Nadine Frey, Rodrigo Nunes da Fonseca, Cornelia von Levetzow, Dominik Stappert, Muhammad Salim Hakeemi, Kai H Conrads, Matthias Pechmann, Kristen A Panfilio, Jeremy A Lynch, Siegfried Roth
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/47346
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spelling doaj-d0e8bd9596d0420f838e8226ad7d63652021-05-05T17:58:09ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.47346Fog signaling has diverse roles in epithelial morphogenesis in insectsMatthew Alan Benton0https://orcid.org/0000-0001-7953-0765Nadine Frey1Rodrigo Nunes da Fonseca2Cornelia von Levetzow3Dominik Stappert4Muhammad Salim Hakeemi5Kai H Conrads6Matthias Pechmann7https://orcid.org/0000-0002-0043-906XKristen A Panfilio8https://orcid.org/0000-0002-6417-251XJeremy A Lynch9https://orcid.org/0000-0001-7625-657XSiegfried Roth10https://orcid.org/0000-0001-5772-3558Institute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, Germany; Department of Zoology, University of Cambridge, Cambridge, United KingdomInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, Germany; School of Life Sciences, University of Warwick, Coventry, United KingdomDepartment of Biological Sciences, University of Illinois, Chicago, United StatesInstitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Köln, GermanyThe 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.https://elifesciences.org/articles/47346Triboliumprimordial germcellsmesoderm invaginationcellularisationamniotic cavitygastrulation
collection DOAJ
language English
format Article
sources DOAJ
author Matthew Alan Benton
Nadine Frey
Rodrigo Nunes da Fonseca
Cornelia von Levetzow
Dominik Stappert
Muhammad Salim Hakeemi
Kai H Conrads
Matthias Pechmann
Kristen A Panfilio
Jeremy A Lynch
Siegfried Roth
spellingShingle Matthew Alan Benton
Nadine Frey
Rodrigo Nunes da Fonseca
Cornelia von Levetzow
Dominik Stappert
Muhammad Salim Hakeemi
Kai H Conrads
Matthias Pechmann
Kristen A Panfilio
Jeremy A Lynch
Siegfried Roth
Fog signaling has diverse roles in epithelial morphogenesis in insects
eLife
Tribolium
primordial germcells
mesoderm invagination
cellularisation
amniotic cavity
gastrulation
author_facet Matthew Alan Benton
Nadine Frey
Rodrigo Nunes da Fonseca
Cornelia von Levetzow
Dominik Stappert
Muhammad Salim Hakeemi
Kai H Conrads
Matthias Pechmann
Kristen A Panfilio
Jeremy A Lynch
Siegfried Roth
author_sort Matthew Alan Benton
title Fog signaling has diverse roles in epithelial morphogenesis in insects
title_short Fog signaling has diverse roles in epithelial morphogenesis in insects
title_full Fog signaling has diverse roles in epithelial morphogenesis in insects
title_fullStr Fog signaling has diverse roles in epithelial morphogenesis in insects
title_full_unstemmed Fog signaling has diverse roles in epithelial morphogenesis in insects
title_sort fog signaling has diverse roles in epithelial morphogenesis in insects
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-10-01
description 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.
topic Tribolium
primordial germcells
mesoderm invagination
cellularisation
amniotic cavity
gastrulation
url https://elifesciences.org/articles/47346
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