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Molecular adaptation and resilience of the insect’s nuclear receptor USP
BACKGROUND: The maintenance of biological systems requires plasticity and robustness. The function of the ecdysone receptor, a heterodimer composed of the nuclear receptors ECR (NR1H1) and USP (NR2B4), was maintained in insects despite a dramatic divergence that occurred during the emergence of Meco...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3520820/ https://www.ncbi.nlm.nih.gov/pubmed/23039844 http://dx.doi.org/10.1186/1471-2148-12-199 |
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author | Chaumot, Arnaud Da Lage, Jean-Luc Maestro, Oscar Martin, David Iwema, Thomas Brunet, Frederic Belles, Xavier Laudet, Vincent Bonneton, François |
author_facet | Chaumot, Arnaud Da Lage, Jean-Luc Maestro, Oscar Martin, David Iwema, Thomas Brunet, Frederic Belles, Xavier Laudet, Vincent Bonneton, François |
author_sort | Chaumot, Arnaud |
collection | PubMed |
description | BACKGROUND: The maintenance of biological systems requires plasticity and robustness. The function of the ecdysone receptor, a heterodimer composed of the nuclear receptors ECR (NR1H1) and USP (NR2B4), was maintained in insects despite a dramatic divergence that occurred during the emergence of Mecopterida. This receptor is therefore a good model to study the evolution of plasticity. We tested the hypothesis that selection has shaped the Ligand-Binding Domain (LBD) of USP during evolution of Mecopterida. RESULTS: We isolated usp and cox1 in several species of Drosophilidae, Tenebrionidae and Blattaria and estimated non-synonymous/synonymous rate ratios using maximum-likelihood methods and codon-based substitution models. Although the usp sequences were mainly under negative selection, we detected relaxation at residues located on the surface of the LBD within Mecopterida families. Using branch-site models, we also detected changes in selective constraints along three successive branches of the Mecopterida evolution. Residues located at the bottom of the ligand-binding pocket (LBP) underwent strong positive selection during the emergence of Mecopterida. This change is correlated with the acquisition of a large LBP filled by phospholipids that probably allowed the stabilisation of the new Mecopterida structure. Later, when the two subgroups of Mecopterida (Amphiesmenoptera: Lepidoptera, Trichoptera; Antliophora: Diptera, Mecoptera, Siphonaptera) diverged, the same positions became under purifying selection. Similarly, several positions of the heterodimerisation interface experienced positive selection during the emergence of Mecopterida, rapidly followed by a phase of constrained evolution. An enlargement of the heterodimerisation surface is specific for Mecopterida and was associated with a reinforcement of the obligatory partnership between ECR and USP, at the expense of homodimerisation. CONCLUSIONS: In order to explain the episodic mode of evolution of USP, we propose a model in which the molecular adaptation of this protein is seen as a process of resilience for the maintenance of the ecdysone receptor functionality. |
format | Online Article Text |
id | pubmed-3520820 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-35208202012-12-13 Molecular adaptation and resilience of the insect’s nuclear receptor USP Chaumot, Arnaud Da Lage, Jean-Luc Maestro, Oscar Martin, David Iwema, Thomas Brunet, Frederic Belles, Xavier Laudet, Vincent Bonneton, François BMC Evol Biol Research Article BACKGROUND: The maintenance of biological systems requires plasticity and robustness. The function of the ecdysone receptor, a heterodimer composed of the nuclear receptors ECR (NR1H1) and USP (NR2B4), was maintained in insects despite a dramatic divergence that occurred during the emergence of Mecopterida. This receptor is therefore a good model to study the evolution of plasticity. We tested the hypothesis that selection has shaped the Ligand-Binding Domain (LBD) of USP during evolution of Mecopterida. RESULTS: We isolated usp and cox1 in several species of Drosophilidae, Tenebrionidae and Blattaria and estimated non-synonymous/synonymous rate ratios using maximum-likelihood methods and codon-based substitution models. Although the usp sequences were mainly under negative selection, we detected relaxation at residues located on the surface of the LBD within Mecopterida families. Using branch-site models, we also detected changes in selective constraints along three successive branches of the Mecopterida evolution. Residues located at the bottom of the ligand-binding pocket (LBP) underwent strong positive selection during the emergence of Mecopterida. This change is correlated with the acquisition of a large LBP filled by phospholipids that probably allowed the stabilisation of the new Mecopterida structure. Later, when the two subgroups of Mecopterida (Amphiesmenoptera: Lepidoptera, Trichoptera; Antliophora: Diptera, Mecoptera, Siphonaptera) diverged, the same positions became under purifying selection. Similarly, several positions of the heterodimerisation interface experienced positive selection during the emergence of Mecopterida, rapidly followed by a phase of constrained evolution. An enlargement of the heterodimerisation surface is specific for Mecopterida and was associated with a reinforcement of the obligatory partnership between ECR and USP, at the expense of homodimerisation. CONCLUSIONS: In order to explain the episodic mode of evolution of USP, we propose a model in which the molecular adaptation of this protein is seen as a process of resilience for the maintenance of the ecdysone receptor functionality. BioMed Central 2012-10-05 /pmc/articles/PMC3520820/ /pubmed/23039844 http://dx.doi.org/10.1186/1471-2148-12-199 Text en Copyright ©2012 Chaumot et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Article Chaumot, Arnaud Da Lage, Jean-Luc Maestro, Oscar Martin, David Iwema, Thomas Brunet, Frederic Belles, Xavier Laudet, Vincent Bonneton, François Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title | Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title_full | Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title_fullStr | Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title_full_unstemmed | Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title_short | Molecular adaptation and resilience of the insect’s nuclear receptor USP |
title_sort | molecular adaptation and resilience of the insect’s nuclear receptor usp |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3520820/ https://www.ncbi.nlm.nih.gov/pubmed/23039844 http://dx.doi.org/10.1186/1471-2148-12-199 |
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