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Open Access Research article

Molecular adaptation and resilience of the insect’s nuclear receptor USP

Arnaud Chaumot2, Jean-Luc Da Lage3, Oscar Maestro4, David Martin4, Thomas Iwema5, Frederic Brunet1, Xavier Belles4, Vincent Laudet1 and François Bonneton1*

Author affiliations

1 Institut de Génomique Fonctionnelle de Lyon (IGFL), Université de Lyon, Université Lyon 1; CNRS; INRA; Ecole Normale Supérieure de Lyon, 32-34 avenue Tony Garnier, Lyon, 69007, France

2 Irstea, UR MALY, Lyon, F-69336, France

3 UPR9034, Laboratoire Evolution, génomes et spéciation (LEGS), CNRS, Gif sur Yvette, 91198, France

4 Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta 37, Barcelona, 08003, Spain

5 Groupe de recherche "immunopathologie et maladies infectieuses (GRI), Universite de la Réunion, Centre CYROI, Cyclotron Réunion Ocean Indien, Sainte Clotilde Ile de la Réunion, 97491, France

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Citation and License

BMC Evolutionary Biology 2012, 12:199  doi:10.1186/1471-2148-12-199

Published: 5 October 2012

Abstract

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.

Keywords:
Nuclear receptors; Ecdysone receptor; ECR; USP; Mecopterida; Selection