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

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...
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Autor*in:	Matthew P Bostock [verfasserIn] Anadika R Prasad [verfasserIn] Alicia Donoghue [verfasserIn] Vilaiwan M Fernandes [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2022

Schlagwörter:	hedgehog morphogen neuronal diversity visual system

Übergeordnetes Werk:	In: eLife - eLife Sciences Publications Ltd, 2013, 11(2022)
Übergeordnetes Werk:	volume:11 ; year:2022

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.7554/eLife.78093

Katalog-ID:	DOAJ033866317

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callnumber-first	Q - Science
author	Matthew P Bostock
spellingShingle	Matthew P Bostock misc QH301-705.5 misc hedgehog misc morphogen misc neuronal diversity misc visual system misc Medicine misc R misc Science misc Q misc Biology (General) Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
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topic_title	QH301-705.5 Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila hedgehog morphogen neuronal diversity visual system
topic	misc QH301-705.5 misc hedgehog misc morphogen misc neuronal diversity misc visual system misc Medicine misc R misc Science misc Q misc Biology (General)
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title	Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
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title_full	Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
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title_sort	photoreceptors generate neuronal diversity in their target field through a hedgehog morphogen gradient in drosophila
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title_auth	Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
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 Hh. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.
abstractGer	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 Hh. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.
abstract_unstemmed	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 Hh. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.
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title_short	Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila
url	https://doi.org/10.7554/eLife.78093 https://doaj.org/article/c7d2bef8127d4df989fd517fa9a02f09 https://elifesciences.org/articles/78093 https://doaj.org/toc/2050-084X
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Photoreceptors generate neuronal diversity in their target field through a Hedgehog morphogen gradient in Drosophila

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