Lineage mapping identifies molecular and architectural similarities between the larval and adult Drosophila central nervous system.

Haluk Lacin,James W Truman

doi:10.7554/elife.13399

Abstract

Neurogenesis in Drosophila occurs in two phases, embryonic and post-embryonic, in which the same set of neuroblasts give rise to the distinct larval and adult nervous systems, respectively. Here, we identified the embryonic neuroblast origin of the adult neuronal lineages in the ventral nervous system via lineage-specific GAL4 lines and molecular markers. Our lineage mapping revealed that neurons born late in the embryonic phase show axonal morphology and transcription factor profiles that are similar to the neurons born post-embryonically from the same neuroblast. Moreover, we identified three thorax-specific neuroblasts not previously characterized and show that HOX genes confine them to the thoracic segments. Two of these, NB2-3 and NB3-4, generate leg motor neurons. The other neuroblast is novel and appears to have arisen recently during insect evolution. Our findings provide a comprehensive view of neurogenesis and show how proliferation of individual neuroblasts is dictated by temporal and spatial cues.

Highlights

IntroductionThe embryonic ventral nerve cord (VNC) of Drosophila has been used as a model system for over three decades to understand how a small number of neuronal stem cells, called neuroblasts (NBs), generate a highly complex but organized tissue in which almost all cells adopt unique fates (Jimenez and Campos-Ortega, 1979; Cabrera et al, 1987; Doe, CQ 1992; Skeath and Carroll, 1992; Bossing et al, 1996; Schmidt et al, 1997; 1999; Rickert et al, 2011)
We proposed that NB5-7 evolved from a duplication of NB5-4 in the thoracic segments for the following reasons: (i) NB5-7 and NB5-4 are similar in terms of their molecular marker expression; (ii) their postembryonic progeny project their axons in a similar manner (Truman et al, 2004); and (iii) these two lineages were the most tightly correlated among all postembryonic lineages with regard to enhancer expression, suggesting that they share the most genes in common (Li et al, 2015)
We have used a suite of molecular markers and a library of GAL4 lines, many of which are specific to individual NBs, to characterize the entire set of thoracic NBs, including their embryonic and postembryonic progeny

Summary

Introduction

The embryonic ventral nerve cord (VNC) of Drosophila has been used as a model system for over three decades to understand how a small number of neuronal stem cells, called neuroblasts (NBs), generate a highly complex but organized tissue in which almost all cells adopt unique fates (Jimenez and Campos-Ortega, 1979; Cabrera et al, 1987; Doe, CQ 1992; Skeath and Carroll, 1992; Bossing et al, 1996; Schmidt et al, 1997; 1999; Rickert et al, 2011). Recent studies have shown that many NBs in the embryonic VNC undergo the following temporal changes of the transcription factor

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Conclusion