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A single WNT enhancer drives specification and regeneration of the Drosophila wing

Wings have provided an evolutionary advantage to insects and have allowed them to diversify. Here, we have identified in Drosophila a highly robust regulatory mechanism that ensures the specification and growth of the wing not only during normal development but also under stress conditions. We prese...

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Autores principales: Gracia-Latorre, Elena, Pérez, Lidia, Muzzopappa, Mariana, Milán, Marco
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395397/
https://www.ncbi.nlm.nih.gov/pubmed/35995781
http://dx.doi.org/10.1038/s41467-022-32400-2
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author Gracia-Latorre, Elena
Pérez, Lidia
Muzzopappa, Mariana
Milán, Marco
author_facet Gracia-Latorre, Elena
Pérez, Lidia
Muzzopappa, Mariana
Milán, Marco
author_sort Gracia-Latorre, Elena
collection PubMed
description Wings have provided an evolutionary advantage to insects and have allowed them to diversify. Here, we have identified in Drosophila a highly robust regulatory mechanism that ensures the specification and growth of the wing not only during normal development but also under stress conditions. We present evidence that a single wing-specific enhancer in the wingless gene is used in two consecutive developmental stages to first drive wing specification and then contribute to mediating the remarkable regenerative capacity of the developing wing upon injury. We identify two evolutionary conserved cis-regulatory modules within this enhancer that are utilized in a redundant manner to mediate these two activities through the use of distinct molecular mechanisms. Whereas Hedgehog and EGFR signalling regulate Wingless expression in early primordia, thus inducing wing specification from body wall precursors, JNK activation in injured tissues induce Wingless expression to promote compensatory proliferation. These results point to evolutionarily linked conservation of wing specification and regeneration to ensure robust development of the wing, perhaps the most relevant evolutionary novelty in insects.
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spelling pubmed-93953972022-08-24 A single WNT enhancer drives specification and regeneration of the Drosophila wing Gracia-Latorre, Elena Pérez, Lidia Muzzopappa, Mariana Milán, Marco Nat Commun Article Wings have provided an evolutionary advantage to insects and have allowed them to diversify. Here, we have identified in Drosophila a highly robust regulatory mechanism that ensures the specification and growth of the wing not only during normal development but also under stress conditions. We present evidence that a single wing-specific enhancer in the wingless gene is used in two consecutive developmental stages to first drive wing specification and then contribute to mediating the remarkable regenerative capacity of the developing wing upon injury. We identify two evolutionary conserved cis-regulatory modules within this enhancer that are utilized in a redundant manner to mediate these two activities through the use of distinct molecular mechanisms. Whereas Hedgehog and EGFR signalling regulate Wingless expression in early primordia, thus inducing wing specification from body wall precursors, JNK activation in injured tissues induce Wingless expression to promote compensatory proliferation. These results point to evolutionarily linked conservation of wing specification and regeneration to ensure robust development of the wing, perhaps the most relevant evolutionary novelty in insects. Nature Publishing Group UK 2022-08-22 /pmc/articles/PMC9395397/ /pubmed/35995781 http://dx.doi.org/10.1038/s41467-022-32400-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Gracia-Latorre, Elena
Pérez, Lidia
Muzzopappa, Mariana
Milán, Marco
A single WNT enhancer drives specification and regeneration of the Drosophila wing
title A single WNT enhancer drives specification and regeneration of the Drosophila wing
title_full A single WNT enhancer drives specification and regeneration of the Drosophila wing
title_fullStr A single WNT enhancer drives specification and regeneration of the Drosophila wing
title_full_unstemmed A single WNT enhancer drives specification and regeneration of the Drosophila wing
title_short A single WNT enhancer drives specification and regeneration of the Drosophila wing
title_sort single wnt enhancer drives specification and regeneration of the drosophila wing
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9395397/
https://www.ncbi.nlm.nih.gov/pubmed/35995781
http://dx.doi.org/10.1038/s41467-022-32400-2
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