Bridging the gap between postembryonic cell lineages and identified embryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster.

Oliver Birkholz,Ivo C Coban,Gerhard M Technau,Julia Nowak,Christof Rickert

doi:10.1242/bio.201411072

Abstract

The clarification of complete cell lineages, which are produced by specific stem cells, is fundamental for understanding mechanisms, controlling the generation of cell diversity and patterning in an emerging tissue. In the developing Central Nervous System (CNS) of Drosophila, neural stem cells (neuroblasts) exhibit two periods of proliferation: During embryogenesis they produce primary lineages, which form the larval CNS. After a phase of mitotic quiescence, a subpopulation of them resumes proliferation in the larva to give rise to secondary lineages that build up the CNS of the adult fly. Within the ventral nerve cord (VNC) detailed descriptions exist for both primary and secondary lineages. However, while primary lineages have been linked to identified neuroblasts, the assignment of secondary lineages has so far been hampered by technical limitations. Therefore, primary and secondary neural lineages co-existed as isolated model systems. Here we provide the missing link between the two systems for all lineages in the thoracic and abdominal neuromeres. Using the Flybow technique, embryonic neuroblasts were identified by their characteristic and unique lineages in the living embryo and their further development was traced into the late larval stage. This comprehensive analysis provides the first complete view of which embryonic neuroblasts are postembryonically reactivated along the anterior/posterior-axis of the VNC, and reveals the relationship between projection patterns of primary and secondary sublineages.

Highlights

Neural stem cells give rise to typical sets of daughter cells, known as lineages or cell clones, which often comprise many different cell types
The strategy we designed for direct tracing of all embryonic neural cell lineages in the ventral nerve cord (VNC) into the late third larval instar requires their in vivo-identification in the embryo (Fig. 1A,B)
This allowed us to bridge the gap between primary and secondary lineages in the VNC. Both of these had been previously described in detail, but so far they appeared as separate model systems for larval and adult Central Nervous System (CNS) development, respectively

Summary

Introduction

Neural stem cells give rise to typical sets of daughter cells, known as lineages or cell clones, which often comprise many different cell types. The identification and precise description of these lineages is the basis to both understanding how cellular diversity and patterning is achieved in the developing CNS and how the individual lineages (developmental units) contribute to the establishment of neural circuits (functional units). All embryonic cell clones of the VNC have been described in detail and each of them is rather invariant, unique and characteristic for a specific NB (Bossing and Technau, 1994; Bossing et al, 1996b; Schmid et al, 1999; Schmidt et al, 1997)

Methods

Results

Discussion

Conclusion