ABSTRACT
A conserved feature of the central nervous system (CNS) is the prominent expansion of anterior regions (brain) compared with posterior (nerve cord). The cellular and regulatory processes driving anterior CNS expansion are not well understood in any bilaterian species. Here, we address this expansion in Drosophila and mouse. We find that, compared with the nerve cord, the brain displays extended progenitor proliferation, more elaborate daughter cell proliferation and more rapid cell cycle speed in both Drosophila and mouse. These features contribute to anterior CNS expansion in both species. With respect to genetic control, enhanced brain proliferation is severely reduced by ectopic Hox gene expression, by either Hox misexpression or by loss of Polycomb group (PcG) function. Strikingly, in PcG mutants, early CNS proliferation appears to be unaffected, whereas subsequent brain proliferation is severely reduced. Hence, a conserved PcG-Hox program promotes the anterior expansion of the CNS. The profound differences in proliferation and in the underlying genetic mechanisms between brain and nerve cord lend support to the emerging concept of separate evolutionary origins of these two CNS regions.
Footnotes
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: B.Y.S., S.T.; Methodology: B.Y.S., I.M.C., J.R., S.T.; Software: I.M.C., J.R.; Formal analysis: B.Y.S., I.M.C., J.R., S.B., J.R.C., A.S.; Investigation: B.Y.S., I.M.C., J.R., S.B., J.R.C., A.S., S.T.; Resources: S.T.; Data curation: B.Y.S., I.M.C., J.R., S.B., J.R.C.; Writing - original draft: B.Y.S., I.M.C., J.R., S.T.; Supervision: S.T.; Project administration: S.T.; Funding acquisition: S.T.
Funding
Funding was provided by the Swedish Research Council (Vetenskapsrådet; 621-2013-5258), the Knut and Alice Wallenberg Foundation (Knut och Alice Wallenbergs Stiftelse; KAW2011.0165 and KAW2012.0101) and the Swedish Cancer Foundation (Cancerfonden; 140780 and 150663) to S.T.
Data availability
RNA-seq data have been deposited in Gene Expression Omnibus under accession numbers GSE111324 (Drosophila) and GSE111232 (mouse).
Supplementary information
Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.160747.supplemental
- Received October 19, 2017.
- Accepted February 24, 2018.
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