1. Developmental Biology
  2. Evolutionary Biology

An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium

  1. Bicheng He
  2. Marita Buescher
  3. Max Stephen Farnworth
  4. Frederic Strobl
  5. Ernst HK Stelzer
  6. Nikolaus DB Koniszewski
  7. Dominik Muehlen
  8. Gregor Bucher  Is a corresponding author
  1. University of Göttingen, Germany
  2. Goethe Universität, Frankfurt am Main, Germany
https://doi.org/10.7554/eLife.49065
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  1. Bicheng He
  2. Marita Buescher
  3. Max Stephen Farnworth
  4. Frederic Strobl
  5. Ernst HK Stelzer
  6. Nikolaus DB Koniszewski
  7. Dominik Muehlen
  8. Gregor Bucher
(2019)
An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium
eLife 8:e49065.
https://doi.org/10.7554/eLife.49065
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Abstract

The genetic control of anterior brain development is highly conserved throughout animals. For instance, a conserved anterior gene regulatory network specifies the ancestral neuroendocrine center of animals and the apical organ of marine organisms. However, its contribution to the brain in non-marine animals has remained elusive. Here, we study the function of the Tc-foxQ2 forkhead transcription factor, a key regulator of the anterior gene regulatory network of insects. We characterized four distinct types of Tc-foxQ2 positive neural progenitor cells based on differential co-expression with Tc-six3/optix, Tc-six4, Tc-chx/vsx, Tc-nkx2.1/scro, Tc-ey, Tc-rx and Tc-fez1. An enhancer trap line built by genome editing marked Tc-foxQ2 positive neurons, which projected through the primary brain commissure and later through a subset of commissural fascicles. Eventually, they contributed to the central complex. Strikingly, in Tc-foxQ2 RNAi knock-down embryos the primary brain commissure did not split and subsequent development of midline brain structures stalled. Our work establishes foxQ2 as a key regulator of brain midline structures, which distinguish the protocerebrum from segmental ganglia. Unexpectedly, our data suggest that the central complex evolved by integrating neural cells from an ancestral anterior neuroendocrine center.

Data availability

All LSM stacks can be downloaded from the figshare repository (https://figshare.com/account/home#/projects/62939). The construct used for generating the enhancer trap is available from AddGene (#124068). The in vivo imaging data is accessible at Zenodo (10.5281/zenodo.2645645 Dataset DS0001 / "left part" of Figure 6 and Supplementary Movie 1; 10.5281/zenodo.2645657 Dataset DS0002; 10.5281/zenodo.2645665 Dataset DS0003 / "right part" of Figure 6 and Supplementary Movie 2)

The following data sets were generated

Article and author information

Author details

  1. Bicheng He

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Marita Buescher

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Max Stephen Farnworth

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2418-3203

  4. Frederic Strobl

    Buchmann Institute for Molecular Life Sciences (BMLS), Goethe Universität, Frankfurt am Main, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Ernst HK Stelzer

    Buchmann Institute for Molecular Life Sciences (BMLS), Goethe Universität, Frankfurt am Main, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1545-0736

  6. Nikolaus DB Koniszewski

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  7. Dominik Muehlen

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. Gregor Bucher

    Johann Friedrich Blumenbach Institute of Zoology, GZMB, University of Göttingen, Göttingen, Germany
    For correspondence
    gbucher1@uni-goettingen.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4615-6401

Funding

Deutsche Forschungsgemeinschaft (BU1443/10)

  • Gregor Bucher

Chinese Scholarship Council (201406350036)

  • Bicheng He

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

Reviewing Editor

  1. Claude Desplan, New York University, United States

Version history

  1. Received: June 5, 2019
  2. Accepted: October 17, 2019
  3. Accepted Manuscript published: October 18, 2019 (version 1)
  4. Version of Record published: November 7, 2019 (version 2)

Copyright

© 2019, He 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. Bicheng He
  2. Marita Buescher
  3. Max Stephen Farnworth
  4. Frederic Strobl
  5. Ernst HK Stelzer
  6. Nikolaus DB Koniszewski
  7. Dominik Muehlen
  8. Gregor Bucher
(2019)
An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium
eLife 8:e49065.
https://doi.org/10.7554/eLife.49065

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