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Ecdysone coordinates plastic growth with robust pattern in the developing wing

Animals develop in unpredictable, variable environments. In response to environmental change, some aspects of development adjust to generate plastic phenotypes. Other aspects of development, however, are buffered against environmental change to produce robust phenotypes. How organ development is coo...

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Autores principales: Nogueira Alves, André, Oliveira, Marisa Mateus, Koyama, Takashi, Shingleton, Alexander, Mirth, Christen Kerry
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947767/
https://www.ncbi.nlm.nih.gov/pubmed/35261337
http://dx.doi.org/10.7554/eLife.72666
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author Nogueira Alves, André
Oliveira, Marisa Mateus
Koyama, Takashi
Shingleton, Alexander
Mirth, Christen Kerry
author_facet Nogueira Alves, André
Oliveira, Marisa Mateus
Koyama, Takashi
Shingleton, Alexander
Mirth, Christen Kerry
author_sort Nogueira Alves, André
collection PubMed
description Animals develop in unpredictable, variable environments. In response to environmental change, some aspects of development adjust to generate plastic phenotypes. Other aspects of development, however, are buffered against environmental change to produce robust phenotypes. How organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we demonstrate that the steroid hormone ecdysone coordinates both plasticity of organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster. Using fed and starved larvae that lack prothoracic glands, which synthesize ecdysone, we show that nutrition regulates growth both via ecdysone and via an ecdysone-independent mechanism, while nutrition regulates patterning only via ecdysone. We then demonstrate that growth shows a graded response to ecdysone concentration, while patterning shows a threshold response. Collectively, these data support a model where nutritionally regulated ecdysone fluctuations confer plasticity by regulating disc growth in response to basal ecdysone levels and confer robustness by initiating patterning only once ecdysone peaks exceed a threshold concentration. This could represent a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change.
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spelling pubmed-89477672022-03-25 Ecdysone coordinates plastic growth with robust pattern in the developing wing Nogueira Alves, André Oliveira, Marisa Mateus Koyama, Takashi Shingleton, Alexander Mirth, Christen Kerry eLife Developmental Biology Animals develop in unpredictable, variable environments. In response to environmental change, some aspects of development adjust to generate plastic phenotypes. Other aspects of development, however, are buffered against environmental change to produce robust phenotypes. How organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we demonstrate that the steroid hormone ecdysone coordinates both plasticity of organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster. Using fed and starved larvae that lack prothoracic glands, which synthesize ecdysone, we show that nutrition regulates growth both via ecdysone and via an ecdysone-independent mechanism, while nutrition regulates patterning only via ecdysone. We then demonstrate that growth shows a graded response to ecdysone concentration, while patterning shows a threshold response. Collectively, these data support a model where nutritionally regulated ecdysone fluctuations confer plasticity by regulating disc growth in response to basal ecdysone levels and confer robustness by initiating patterning only once ecdysone peaks exceed a threshold concentration. This could represent a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change. eLife Sciences Publications, Ltd 2022-03-09 /pmc/articles/PMC8947767/ /pubmed/35261337 http://dx.doi.org/10.7554/eLife.72666 Text en © 2022, Nogueira Alves et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Nogueira Alves, André
Oliveira, Marisa Mateus
Koyama, Takashi
Shingleton, Alexander
Mirth, Christen Kerry
Ecdysone coordinates plastic growth with robust pattern in the developing wing
title Ecdysone coordinates plastic growth with robust pattern in the developing wing
title_full Ecdysone coordinates plastic growth with robust pattern in the developing wing
title_fullStr Ecdysone coordinates plastic growth with robust pattern in the developing wing
title_full_unstemmed Ecdysone coordinates plastic growth with robust pattern in the developing wing
title_short Ecdysone coordinates plastic growth with robust pattern in the developing wing
title_sort ecdysone coordinates plastic growth with robust pattern in the developing wing
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8947767/
https://www.ncbi.nlm.nih.gov/pubmed/35261337
http://dx.doi.org/10.7554/eLife.72666
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