Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
- University College London, United Kingdom
Abstract
Defining the origin of neuronal diversity is a major challenge in developmental neurobiology. The Drosophila visual system is an excellent paradigm to study how cellular diversity is generated. Photoreceptors from the eye disc grow their axons into the optic lobe and secrete Hedgehog (Hh) to induce the lamina, such that for every unit eye there is a corresponding lamina unit made up of post-mitotic precursors stacked into columns. Each differentiated column contains five lamina neuron types (L1-L5), making it the simplest neuropil in the optic lobe, yet how this diversity is generated was unknown. Here, we found that Hh pathway activity is graded along the distal-proximal axis of lamina columns and further determined that this gradient in pathway activity arises from a gradient of Hh ligand. We manipulated Hh pathway activity cell-autonomously in lamina precursors and non-cell autonomously by inactivating the Hh ligand, and by knocking it down in photoreceptors. These manipulations showed that different thresholds of activity specify unique cell identities, with more proximal cell types specified in response to progressively lower Hh levels. Thus, our data establish that Hh acts as a morphogen to pattern the lamina. Although, this is the first such report during Drosophila nervous system development, our work uncovers a remarkable similarity with the vertebrate neural tube, which is patterned by Sonic Hedgehog. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.
Data availability
All data generated or analysed during this study are included in the manuscript
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Neuronal diversity and convergence in a visual system developmental atlasNCBI Gene Expression Omnibus, GSE142789.
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Transcriptional programs of circuit assembly in the Drosophila visual systemNCBI Gene Expression Omnibus, GSE156455.
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A comprehensive series of temporal transcription factors in the fly visual systemNCBI Gene Expression Omnibus, GSE167266.
Article and author information
Author details
Vilaiwan M Fernandes
Funding
Wellcome Trust (210472/Z/18/Z)
- Vilaiwan M Fernandes
University College London (Biosciences Graduate Research Scholarship)
- Matthew P Bostock
University College London (Overseas Research Scholarship and Graduate Research Scholarship)
- Anadika R Prasad
University College London (Research Opportunity Scholarship)
- Alicia Donoghue
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Bostock et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
eLife 11:e78093.
https://doi.org/10.7554/eLife.78093
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