Abstract

The Drosophila brain develops from the procephalic neurogenic region of the ectoderm. About 100 neural precursor cells (neuroblasts) delaminate from this region on either side in a reproducible spatiotemporal pattern. We provide neuroblast maps from different stages of the early embryo (stages 9, 10 and 11, when the entire population of neuroblasts has formed), in which about 40 molecular markers representing the expression patterns of 34 different genes are linked to individual neuroblasts. In particular, we present a detailed description of the spatiotemporal patterns of expression in the procephalic neuroectoderm and in the neuroblast layer of the gap genes empty spiracles, hunchback, huckebein, sloppy paired 1 and tailless; the homeotic gene labial; the early eye genes dachshund, eyeless and twin of eyeless; and several other marker genes (including castor, pdm1, fasciclin 2, klumpfuss, ladybird, runt and unplugged). We show that based on the combination of genes expressed, each brain neuroblast acquires a unique identity, and that it is possible to follow the fate of individual neuroblasts through early neurogenesis. Furthermore, despite the highly derived patterns of expression in the procephalic segments, the co-expression of specific molecular markers discloses the existence of serially homologous neuroblasts in neuromeres of the ventral nerve cord and the brain. Taking into consideration that all brain neuroblasts are now assigned to particular neuromeres and individually identified by their unique gene expression, and that the genes found to be expressed are likely candidates for controlling the development of the respective neuroblasts, our data provide a basic framework for studying the mechanisms leading to pattern and cell diversity in the Drosophila brain, and for addressing those mechanisms that make the brain different from the truncal CNS.

Highlights

  • The central nervous system (CNS) of Drosophila, which encompasses the brain and ventral nerve cord, develops from a bilateral neuroectoderm, which gives rise to multipotent neural stem cells, called neuroblasts (NB)

  • The cephalic gap genes are expressed in large domains of the procephalon and play a crucial role in the patterning of the peripheral ectoderm, and in regionalizing the brain primordium (Hartmann et al, 2000; Hirth et al, 1995; Reichert, 2002; Younossi-Hartenstein et al, 1997)

  • To see whether the cephalic gap genes respect the neuromeric boundaries and to provide a basis for studying their potential role in the formation or specification of brain precursor cells we studied the expression of orthodenticle, empty spiracles, sloppy paired 1, tailless, huckebein, and hunchback in the developing head ectoderm, as well as in the entire population of identified NBs during stages 9-11 (Figs 1, 2)

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Summary

Introduction

The central nervous system (CNS) of Drosophila, which encompasses the brain and ventral nerve cord, develops from a bilateral neuroectoderm, which gives rise to multipotent neural stem cells, called neuroblasts (NB). Experimental data suggest that once NBs are specified, their further development is largely controlled by their intrinsic properties (Brody and Odenwald, 2000; Prokop and Technau, 1994; Udolph et al, 1995). Such intrinsic properties might be established by the distinct combination of genes expressed in a NB (Doe, 1992; Isshiki et al, 2001)

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