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A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless

Development of the Drosophila wing—a paradigm of organ development—is governed by 2 morphogens, Decapentaplegic (Dpp, a BMP) and Wingless (Wg, a Wnt). Both proteins are produced by defined subpopulations of cells and spread outwards, forming gradients that control gene expression and cell pattern as...

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Autores principales: Zecca, Myriam, Struhl, Gary
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8148325/
https://www.ncbi.nlm.nih.gov/pubmed/33657096
http://dx.doi.org/10.1371/journal.pbio.3001111
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author Zecca, Myriam
Struhl, Gary
author_facet Zecca, Myriam
Struhl, Gary
author_sort Zecca, Myriam
collection PubMed
description Development of the Drosophila wing—a paradigm of organ development—is governed by 2 morphogens, Decapentaplegic (Dpp, a BMP) and Wingless (Wg, a Wnt). Both proteins are produced by defined subpopulations of cells and spread outwards, forming gradients that control gene expression and cell pattern as a function of concentration. They also control growth, but how is unknown. Most studies have focused on Dpp and yielded disparate models in which cells throughout the wing grow at similar rates in response to the grade or temporal change in Dpp concentration or to the different amounts of Dpp “equalized” by molecular or mechanical feedbacks. In contrast, a model for Wg posits that growth is governed by a progressive expansion in morphogen range, via a mechanism in which a minimum threshold of Wg sustains the growth of cells within the wing and recruits surrounding “pre-wing” cells to grow and enter the wing. This mechanism depends on the capacity of Wg to fuel the autoregulation of vestigial (vg)—the selector gene that specifies the wing state—both to sustain vg expression in wing cells and by a feed-forward (FF) circuit of Fat (Ft)/Dachsous (Ds) protocadherin signaling to induce vg expression in neighboring pre-wing cells. Here, we have subjected Dpp to the same experimental tests used to elucidate the Wg model and find that it behaves indistinguishably. Hence, we posit that both morphogens act together, via a common mechanism, to control wing growth as a function of morphogen range.
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spelling pubmed-81483252021-06-07 A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless Zecca, Myriam Struhl, Gary PLoS Biol Research Article Development of the Drosophila wing—a paradigm of organ development—is governed by 2 morphogens, Decapentaplegic (Dpp, a BMP) and Wingless (Wg, a Wnt). Both proteins are produced by defined subpopulations of cells and spread outwards, forming gradients that control gene expression and cell pattern as a function of concentration. They also control growth, but how is unknown. Most studies have focused on Dpp and yielded disparate models in which cells throughout the wing grow at similar rates in response to the grade or temporal change in Dpp concentration or to the different amounts of Dpp “equalized” by molecular or mechanical feedbacks. In contrast, a model for Wg posits that growth is governed by a progressive expansion in morphogen range, via a mechanism in which a minimum threshold of Wg sustains the growth of cells within the wing and recruits surrounding “pre-wing” cells to grow and enter the wing. This mechanism depends on the capacity of Wg to fuel the autoregulation of vestigial (vg)—the selector gene that specifies the wing state—both to sustain vg expression in wing cells and by a feed-forward (FF) circuit of Fat (Ft)/Dachsous (Ds) protocadherin signaling to induce vg expression in neighboring pre-wing cells. Here, we have subjected Dpp to the same experimental tests used to elucidate the Wg model and find that it behaves indistinguishably. Hence, we posit that both morphogens act together, via a common mechanism, to control wing growth as a function of morphogen range. Public Library of Science 2021-03-03 /pmc/articles/PMC8148325/ /pubmed/33657096 http://dx.doi.org/10.1371/journal.pbio.3001111 Text en © 2021 Zecca, Struhl https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Zecca, Myriam
Struhl, Gary
A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title_full A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title_fullStr A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title_full_unstemmed A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title_short A unified mechanism for the control of Drosophila wing growth by the morphogens Decapentaplegic and Wingless
title_sort unified mechanism for the control of drosophila wing growth by the morphogens decapentaplegic and wingless
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8148325/
https://www.ncbi.nlm.nih.gov/pubmed/33657096
http://dx.doi.org/10.1371/journal.pbio.3001111
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