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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...

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Autores principales: Chaumot, Arnaud, Da Lage, Jean-Luc, Maestro, Oscar, Martin, David, Iwema, Thomas, Brunet, Frederic, Belles, Xavier, Laudet, Vincent, Bonneton, François
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
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.
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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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