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.
Reviewing Editor
- Claude Desplan, New York University, United States
Version history
- Received: June 5, 2019
- Accepted: October 17, 2019
- Accepted Manuscript published: October 18, 2019 (version 1)
- 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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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
Further reading
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We previously showed that SerpinE2 and the serine protease HtrA1 modulate fibroblast growth factor (FGF) signaling in germ layer specification and head-to-tail development of Xenopus embryos. Here, we present an extracellular proteolytic mechanism involving this serpin-protease system in the developing neural crest (NC). Knockdown of SerpinE2 by injected antisense morpholino oligonucleotides did not affect the specification of NC progenitors but instead inhibited the migration of NC cells, causing defects in dorsal fin, melanocyte, and craniofacial cartilage formation. Similarly, overexpression of the HtrA1 protease impaired NC cell migration and the formation of NC-derived structures. The phenotype of SerpinE2 knockdown was overcome by concomitant downregulation of HtrA1, indicating that SerpinE2 stimulates NC migration by inhibiting endogenous HtrA1 activity. SerpinE2 binds to HtrA1, and the HtrA1 protease triggers degradation of the cell surface proteoglycan Syndecan-4 (Sdc4). Microinjection of Sdc4 mRNA partially rescued NC migration defects induced by both HtrA1 upregulation and SerpinE2 downregulation. These epistatic experiments suggest a proteolytic pathway by a double inhibition mechanism:
SerpinE2 ┤HtrA1 protease ┤Syndecan-4 → NC cell migration.
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Human fetal development has been associated with brain health at later stages. It is unknown whether growth in utero, as indexed by birth weight (BW), relates consistently to lifespan brain characteristics and changes, and to what extent these influences are of a genetic or environmental nature. Here we show remarkably stable and lifelong positive associations between BW and cortical surface area and volume across and within developmental, aging and lifespan longitudinal samples (N = 5794, 4–82 y of age, w/386 monozygotic twins, followed for up to 8.3 y w/12,088 brain MRIs). In contrast, no consistent effect of BW on brain changes was observed. Partly environmental effects were indicated by analysis of twin BW discordance. In conclusion, the influence of prenatal growth on cortical topography is stable and reliable through the lifespan. This early-life factor appears to influence the brain by association of brain reserve, rather than brain maintenance. Thus, fetal influences appear omnipresent in the spacetime of the human brain throughout the human lifespan. Optimizing fetal growth may increase brain reserve for life, also in aging.
