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

  1. Matthew Alan Benton

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7953-0765
  2. Nadine Frey

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Rodrigo Nunes da Fonseca

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Cornelia von Levetzow

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Dominik Stappert

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Muhammad Salim Hakeemi

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Kai H Conrads

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Matthias Pechmann

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0043-906X
  9. Kristen A Panfilio

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6417-251X
  10. Jeremy A Lynch

    Department of Biological Sciences, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7625-657X
  11. Siegfried Roth

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    For correspondence
    siegfried.roth@uni-koeln.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5772-3558

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

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Version history

  1. Received: April 2, 2019
  2. Accepted: September 30, 2019
  3. Accepted Manuscript published: October 1, 2019 (version 1)
  4. 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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  1. Matthew Alan Benton
  2. Nadine Frey
  3. Rodrigo Nunes da Fonseca
  4. Cornelia von Levetzow
  5. Dominik Stappert
  6. Muhammad Salim Hakeemi
  7. Kai H Conrads
  8. Matthias Pechmann
  9. Kristen A Panfilio
  10. Jeremy A Lynch
  11. Siegfried Roth
(2019)
Fog signaling has diverse roles in epithelial morphogenesis in insects
eLife 8:e47346.
https://doi.org/10.7554/eLife.47346

Share this article

https://doi.org/10.7554/eLife.47346

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