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

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.DOI: http://dx.doi.org/10.7554/eLife.13399.001

Differing Strategies Despite Shared Lineages of Motor Neurons and Glia to Achieve Robust Development of an Adult Neuropil in Drosophila

“…Although each motor neuron morphology is thought to be determined by unique combinations of morphology transcription factors (mTFs; Enriquez et al, 2015), how these stereotyped morphologies form the correct synaptic connections with interneurons and sensory neurons is not understood. Interestingly, at least one of the major NB lineages that give rise to adult motor neurons in the fly also generates another important cell type in the nervous system, glia (Baek et al, 2013; Lacin and Truman, 2016), which are critical for the establishment of synapses and the maintenance of neuronal activity (Freeman, 2015; Freeman and Rowitch, 2013). The observation that glia and leg motor neurons may be derived from common progenitors (neuroglioblast [NGB]) raised the possibility that their development may be coordinated, and that being born from the same lineages might also play a role in neural circuit assembly.…”

Unique patterns of organization and migration of FGF-expressing cells during Drosophila morphogenesis

“…Secondly, the late-stage (stage 13) expression of bnl in neurons matched the timing of delamination of NB 4-4 (S4), rather than NB 3-5 (S1). Finally, similar to the NB 4-4 lineage (Lacin and Truman, 2016), the bnl -expressing neurons were found in all thoracic and abdominal segments, both had interneuron and motor neuron projections in the thoracic segments, and they induced apoptosis toward late embryogenesis and were not marked by Ems in the abdominal hemisegments (Fig. 6O-R).…”

“…Considering all these expression patterns and the stereotyped arrangement of embryonic NBs (Doe, 1992), bnl -expressing neurons were predicted to be either from the NB 4-4 or NB 3-5 lineage. Positive immunostaining for Ems ( empty spiracles ), a marker for NB 3-5, and 4-4 (Lacin and Truman, 2016) confirmed that the bnl -expressing neurons are either NB 3-5 or 4-4 (Fig. 6P-P″).…”

“…S4H,J), but subcellular localization of the signal detected by these methods did not reveal a neuronal morphology. Engrailed, a marker for NB 6 and 7(Broadus et al, 1995), Hb9 (Extra-extra), a marker for NB 1-1, 1-2, 2-2, 3-1, 3-2, and 5-2 (Lacin and Truman, 2016), and the eagle-Gal4 line that marks NB 2-4 and 3-3 (Higashijima et al, 1996) did not localize in bnl -neurons (Fig. S4K-M).…”

“…Our analyses of bnl-LexA expression identified the NB 4-4 derived bnl expressing neurons in embryonic CNS. A recent study (Lacin and Truman, 2016) linked the embryonic NB 4-4 lineage to their corresponding post-embryonic progenitors and also showed that the thoracic NB 4-4 lineage generates the leg motor neurons.…”