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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
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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. |
format | Online Article Text |
id | pubmed-8947767 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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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