Neuroblast pattern and identity in the Drosophila tail region and role of doublesex in the survival of sex-specific precursors

Abstract

SUMMARYThe central nervous system is composed of segmental units (neuromeres), the size and complexity of which evolved in correspondence to their functional requirements. In Drosophila, neuromeres develop from populations of neural stem cells (neuroblasts) that delaminate from the early embryonic neuroectoderm in a stereotyped spatial and temporal pattern. Pattern units closely resemble the ground state and are rather invariant in thoracic (T1-T3) and anterior abdominal (A1-A7) segments of the embryonic ventral nerve cord. Here, we provide a comprehensive neuroblast map of the terminal abdominal neuromeres A8-A10, which exhibit a progressively derived character. Compared with thoracic and anterior abdominal segments, neuroblast numbers are reduced by 28% in A9 and 66% in A10 and are almost entirely absent in the posterior compartments of these segments. However, all neuroblasts formed exhibit serial homology to their counterparts in more anterior segments and are individually identifiable based on their combinatorial code of marker gene expression, position, delamination time point and the presence of characteristic progeny cells. Furthermore, we traced the embryonic origin and characterised the postembryonic lineages of a set of terminal neuroblasts, which have been previously reported to exhibit sex-specific proliferation behaviour during postembryonic development. We show that the respective sex-specific product of the gene doublesex promotes programmed cell death of these neuroblasts in females, and is needed for their survival, but not proliferation, in males. These data establish the terminal neuromeres as a model for further investigations into the mechanisms controlling segment-and sex-specific patterning in the central nervous system.

Female-biased dimorphism underlies a female-specific role for post-embryonic Ilp7 neurons inDrosophilafertility

“…Many SAbg neurons are lost in dsx-null males, and a subset is gained in dsxnull females (Billeter et al, 2006). Underlying this is the induction of female-specific programmed cell death of posterior neuroblast lineages in females by DsxF, and their survival and lineage progression in males due to DsxM (Taylor and Truman, 1992;Billeter et al, 2006;Birkholz et al, 2013). The function of fruM is thereafter limited to activating serotonin expression in the remaining neurons (Billeter et al, 2006).…”

Specification of neuronal subtypes by different levels of Hunchback

“…S1A-C) (Birkholz et al, 2013). We excluded NB3-3, as CCAP neurons do not express eagle (eg)-Gal4>UAS-GFP and it has been shown that eg expression is maintained by the NB3-3 lineage at least until late embryogenesis ( Fig.…”

sequoia controls the type I>0 daughter proliferation switch in the developing Drosophila nervous system

“…1A) (Bossing et al, 1996;Schmidt et al, 1997Schmidt et al, , 1999Urbach et al, 2003Urbach et al, , 2016Wheeler et al, 2009;Birkholz et al, 2013). The CNS can be subdivided into the brain and the ventral nerve cord (VNC); here, we focus on the VNC.…”