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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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 |
work_keys_str_mv |
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1721458903872438272 |