1. Developmental Biology
  2. Neuroscience

Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila

  1. Matthew P Bostock
  2. Anadika R Prasad
  3. Alicia Donoghue
  4. Vilaiwan M Fernandes  Is a corresponding author
  1. University College London, United Kingdom
https://doi.org/10.7554/eLife.78093
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  1. Matthew P Bostock
  2. Anadika R Prasad
  3. Alicia Donoghue
  4. Vilaiwan M Fernandes
(2022)
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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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

The following previously published data sets were used

Article and author information

Author details

  1. Matthew P Bostock

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.

  2. Anadika R Prasad

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.

  3. Alicia Donoghue

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.

  4. Vilaiwan M Fernandes

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    For correspondence
    vilaiwan.fernandes@ucl.ac.uk
    Competing interests
    Vilaiwan M Fernandes, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1991-7252

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.

Reviewing Editor

  1. Sonia Sen, Tata Institute for Genetics and Society, India

Version history

  1. Preprint posted: February 22, 2022 (view preprint)
  2. Received: February 22, 2022
  3. Accepted: August 23, 2022
  4. Accepted Manuscript published: August 25, 2022 (version 1)
  5. Version of Record published: September 23, 2022 (version 2)

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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  1. Matthew P Bostock
  2. Anadika R Prasad
  3. Alicia Donoghue
  4. Vilaiwan M Fernandes
(2022)
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

Share this article

https://doi.org/10.7554/eLife.78093

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