Molecular adaptation and resilience of the insect’s nuclear receptor USP
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
BMC Evolutionary Biology 2012, 12:199 doi:10.1186/1471-2148-12-199Published: 5 October 2012
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.
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.
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.