Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network

  1. Matthias Pechmann  Is a corresponding author
  2. Nathan James Kenny
  3. Laura Pott
  4. Peter Heger
  5. Yen-Ta Chen
  6. Thomas Buchta
  7. Orhan Özüak
  8. Jeremy A Lynch
  9. Siegfried Roth  Is a corresponding author
  1. University of Cologne, Germany
  2. The Natural History Museum, United Kingdom
  3. University of Illinois at Chicago, United States

Abstract

Dorsoventral pattering relies on Toll and BMP signalling in all insects studied so far, with variations in the relative contributions of both pathways. Drosophila and the beetle Tribolium share extensive dependence on Toll, while representatives of more distantly related lineages like the wasp Nasonia and bug Oncopeltus rely more strongly on BMP signalling. Here, we show that in the cricket Gryllus bimaculatus, an evolutionarily distant outgroup, Toll has, like in Drosophila, a direct patterning role for the ventral half of the embryo. In addition, Toll polarizes BMP signalling, although this does not involve the conserved BMP inhibitor Sog/Chordin. Finally, Toll activation relies on ovarian patterning mechanisms with striking similarity to Drosophila. Our data suggest two surprising hypotheses: 1) that Toll's patterning function in Gryllus and Drosophila is the result of convergent evolution or 2) a Drosophila-like system arose early in insect evolution, and was extensively altered in multiple independent lineages.

Data availability

Raw reads from our sequencing are available from the NCBI SRA under accession PRJNA492804The Gryllus transcriptome is available from 10.6084/m9.figshare.14211062

The following data sets were generated

Article and author information

Author details

  1. Matthias Pechmann

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    For correspondence
    pechmanm@uni-koeln.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0043-906X
  2. Nathan James Kenny

    Life Sciences Department, The Natural History Museum, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4816-4103
  3. Laura Pott

    Insitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3314-6239
  4. Peter Heger

    Institute for Genetics, University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2583-2981
  5. Yen-Ta Chen

    Institute for Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Thomas Buchta

    Insitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Orhan Özüak

    Insitute for Zoology/Developmental Biology, Biocenter, University of Cologne, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. 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
  9. 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

University of Cologne (Postdoc grant)

  • Matthias Pechmann

Deutsche Forschungsgemeinschaft (CRC 680)

  • Yen-Ta Chen

Deutsche Forschungsgemeinschaft (CRC 680)

  • Thomas Buchta

Deutsche Forschungsgemeinschaft (CRC 680)

  • Thomas Buchta

Deutsche Forschungsgemeinschaft (CRC 680)

  • Orhan Özüak

Deutsche Forschungsgemeinschaft (CRC 680)

  • Jeremy A Lynch

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Patricia J Wittkopp, University of Michigan, United States

Publication history

  1. Received: March 15, 2021
  2. Accepted: March 24, 2021
  3. Accepted Manuscript published: March 30, 2021 (version 1)
  4. Version of Record published: April 16, 2021 (version 2)

Copyright

© 2021, Pechmann 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. Matthias Pechmann
  2. Nathan James Kenny
  3. Laura Pott
  4. Peter Heger
  5. Yen-Ta Chen
  6. Thomas Buchta
  7. Orhan Özüak
  8. Jeremy A Lynch
  9. Siegfried Roth
(2021)
Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network
eLife 10:e68287.
https://doi.org/10.7554/eLife.68287
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