Dataset Information

Molecular evolution of ultraspiracle protein (USP/RXR) in insects.

ABSTRACT: Ultraspiracle protein/retinoid X receptor (USP/RXR) is a nuclear receptor and transcription factor which is an essential component of a heterodimeric receptor complex with the ecdysone receptor (EcR). In insects this complex binds ecdysteroids and plays an important role in the regulation of growth, development, metamorphosis and reproduction. In some holometabolous insects, including Lepidoptera and Diptera, USP/RXR is thought to have experienced several important shifts in function. These include the acquisition of novel ligand-binding properties and an expanded dimerization interface with EcR. In light of these recent hypotheses, we implemented codon-based likelihood methods to investigate if the proposed shifts in function are reflected in changes in site-specific evolutionary rates across functional and structural motifs in insect USP/RXR sequences, and if there is any evidence for positive selection at functionally important sites. Our results reveal evidence of positive selection acting on sites within the loop connecting helices H1 and H3, the ligand-binding pocket, and the dimer interface in the holometabolous lineage leading to the Lepidoptera/Diptera/Trichoptera. Similar analyses conducted using EcR sequences did not indicate positive selection. However, analyses allowing for variation across sites demonstrated elevated non-synonymous/synonymous rate ratios (d(N)/d(S)), suggesting relaxed constraint, within the dimerization interface of both USP/RXR and EcR as well as within the coactivator binding groove and helix H12 of USP/RXR. Since the above methods are based on the assumption that d(S) is constant among sites, we also used more recent models which relax this assumption and obtained results consistent with traditional random-sites models. Overall our findings support the evolution of novel function in USP/RXR of more derived holometabolous insects, and are consistent with shifts in structure and function which may have increased USP/RXR reliance on EcR for cofactor recruitment. Moreover, these findings raise important questions regarding hypotheses which suggest the independent activation of USP/RXR by its own ligand.

SUBMITTER: Hult EF

PROVIDER: S-EPMC3162005 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Molecular evolution of ultraspiracle protein (USP/RXR) in insects.

Hult Ekaterina F EF Tobe Stephen S SS Chang Belinda S W BS

PloS one 20110825 8

Ultraspiracle protein/retinoid X receptor (USP/RXR) is a nuclear receptor and transcription factor which is an essential component of a heterodimeric receptor complex with the ecdysone receptor (EcR). In insects this complex binds ecdysteroids and plays an important role in the regulation of growth, development, metamorphosis and reproduction. In some holometabolous insects, including Lepidoptera and Diptera, USP/RXR is thought to have experienced several important shifts in function. These incl ...[more]

PMID: 21901121

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Project description:Conopomorpha sinensis Bradley (Lepidoptera: Gracilariidae) is the dominant insect pest of litchi (chinensis Sonn.) and longan (Euphoria longan Lour.) fruit trees. Management of this pest species is a challenging task due to its cryptic borer behavior. Controlling C. sinensis at the egg stage is the best alternative strategy to chemical control of C. sinensis adults. However, thorough studies regarding the indirect and sublethal effects of chemicals on the different developmental stages of C. sinensis are insufficient. In this study, the effect of some insecticides was evaluated on C. sinensis eggs. The ovicidal activity of chlorbenzuron, abamectin, chlorantraniliprole, and λ-cyhalothrin was confirmed by morphological observation of the defects in C. sinensis eggs. Moreover, we characterized four essential ecdysone receptor proteins in insects [i.e., two isoform ecdysone receptors (EcR: CsEcRA. CsEcRB) and two isoform ultraspiracle proteins (USP: CsUSP1, CsUSP2)] from C. sinensis eggs. The CsEcRA, CsEcRB, CsUSP1, and CsUSP2 genes consisted of 1521-, 1614-, 1410-, and 1236-bp open reading frames which encoded proteins of 506, 527, 469, and 413 amino acid residues, respectively. Furthermore, the embryonic differential responses of CsEcRs, CsUSPs, and vitellogenin receptor (VgR: CsVgR) to insecticides were evaluated by qRT-PCR. Among the five tested genes, CsVgR and CsUSP1 were the most sensitive to all the tested insecticides, with fold change of the expression diminished by 4.27-8.70 times compared with untreated control insects. The data suggests that these insecticidal compounds regulate the expression of these specific proteins, which might eventually lead to reduced viability of C. sinensis eggs. We present here the first data providing molecular elucidation of ecdysone receptor genes and their differential responses to insecticides in C. sinensis eggs. Together with our previous report of insecticide sublethal effects on two reproduction-related genes in C. sinensis adults, CsVgR and CsUSP1 seem to be appropriate molecular parameters for the evaluation of insecticide impact on C. sinensis. This study exemplifies the potential utility of transcriptional measurement of nuclear receptors as the molecular biomarkers for ecotoxicological evaluations of ovicidal impact of insecticides.

Project description:BackgroundThe 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.ResultsWe 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.ConclusionsIn 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.

Dataset Information

Molecular evolution of ultraspiracle protein (USP/RXR) in insects.

Publications

Molecular evolution of ultraspiracle protein (USP/RXR) in insects.

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