An ancestral apical brain region contributes to the central complex under the control of foxQ2 in the beetle Tribolium
- University of Göttingen, Germany
- Goethe Universität, Frankfurt am Main, Germany
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)
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In vivo imaging of foxQ2 postitive neurons in the beetle Tribolium castaneum (10X)Zenodo, 10.5281/zenodo.2645645.
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In vivo imaging of foxQ2 postitive neurons in the beetle Tribolium castaneum (40X)Zenodo, 10.5281/zenodo.2645657 Dataset DS0002.
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In vivo imaging of foxQ2 postitive neurons in the beetle Tribolium castaneumZenodo, 10.5281/zenodo.2645665 Dataset DS0003.
Article and author information
Author details
Max Stephen Farnworth
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.
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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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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