A neural progenitor mitotic wave is required for asynchronous axon outgrowth and morphology.

Jérôme Lacoste,Sophie Louvet-Vallée,Angélique Burg,Pénélope Darnat,Agnès Audibert,Michel Gho,Hédi Soula

doi:10.7554/elife.75746

Abstract

Spatiotemporal mechanisms generating neural diversity are fundamental for understanding neural processes. Here, we investigated how neural diversity arises from neurons coming from identical progenitors. In the dorsal thorax of Drosophila, rows of mechanosensory organs originate from the division of sensory organ progenitor (SOPs). We show that in each row of the notum, an anteromedial located central SOP divides first, then neighbouring SOPs divide, and so on. This centrifugal wave of mitoses depends on cell-cell inhibitory interactions mediated by SOP cytoplasmic protrusions and Scabrous, a secreted protein interacting with the Delta/Notch complex. Furthermore, when this mitotic wave was reduced, axonal growth was more synchronous, axonal terminals had a complex branching pattern and fly behaviour was impaired. We show that the temporal order of progenitor divisions influences the birth order of sensory neurons, axon branching and impact on grooming behaviour. These data support the idea that developmental timing controls axon wiring neural diversity.

Highlights

It is commonly accepted that nervous system development relies on the precise spatio-temporal regulation of gene expression in neural progenitors (Holguera and Desplan, 2018)
To investigate whether Sca is involved in the synchronization of sensory organ progenitor cells (SOPs) mitosis, we studied the mitotic wave in the scaBP2 null mutant, which is viable at the developmental period studied
To study how functional neuronal diversity can be generated from a homogenous set of neural precursors, we took advantage of the invariant way in which sensory organs are located on the dorsal epithelium of Drosophila

Summary

Introduction

It is commonly accepted that nervous system development relies on the precise spatio-temporal regulation of gene expression in neural progenitors (Holguera and Desplan, 2018). Little is known about how neural diversity can be generated among neural progenitors that are homogenously specified (Hirata and Iwai, 2019), for example, in neurons that connect peripheral sensory organs with the central nervous system (Gatto et al, 2019). Microchætes are peripheral mechanosensory organs on the thorax of Drosophila melanogaster. These organs arise from sensory organ progenitor cells (SOPs) which are selected among G2 arrested cells of proneural clusters during pupal stage (Sato et al, 1999; Usui and Kimura, 1993). In the dorsal region of the thorax (notum), SOPs appear sequentially from five parallel proneural rows: first rows 5, followed by rows and 3 and rows 2 and 4 (Usui and Kimura, 1993; Corson et al, 2017).

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Conclusion