Evolution of Nuclear Receptors in Insects

Bonneton, François; Laudet, Vincent

doi:10.1016/b978-0-12-384749-2.10006-8

Cited by 18 publications

(22 citation statements)

References 335 publications

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“…The JH receptor has been long sought, and two major candidates have been put forward: (1) Ultraspiracle (USP), a member of the nuclear hormone receptor family [12,64], that forms a heterodimer with the ecdysone receptor (EcR) to mediate ecdysone action [57];…”

Section: Jh Receptormentioning

confidence: 99%

How does juvenile hormone control insect metamorphosis and reproduction?

Riddiford

2012

General and Comparative Endocrinology

303

187

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Section: Jh Receptormentioning

confidence: 99%

How does juvenile hormone control insect metamorphosis and reproduction?

Riddiford

2012

General and Comparative Endocrinology

303

187

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“…The function of the heterodimer ECR-USP in the ecdysone response is conserved in all insects, including Mecopterida [58]. Therefore, although we cannot exclude the possibility that other biological functions have changed with USP, it seems that adaptation of this protein allowed maintenance rather than innovation.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2012

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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.

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“…First, Broad was one of only two TFs to exhibit a signature of plasticity between more than one pair of behavioral categories in the bioinformatic analysis described above (see Results). Second, Broad is known to be a pleiotropic integrator of diverse endocrine cascades in multiple insect species (Bonneton and Laudet, 2012). It mediates insulin, juvenile hormone (JH) and vitellogenin (Bonneton and Laudet, 2012;Hamilton et al, 2017) signaling, all of which are known to play a causal role in honey bee behavioral maturation (Hamilton et al, 2017;Zayed and Robinson, 2012).…”

Section: Tfs Chosen For Manipulationmentioning

confidence: 99%

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain

Hamilton

Traniello

Ray

et al. 2019

Journal of Experimental Biology

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Studies in evolutionary and developmental biology show that relationships between transcription factors (TFs) and their target genes can be altered to result in novel regulatory relationships that generate phenotypic plasticity. We hypothesized that contextdependent shifts in the nervous system associated with behavior may also be linked to changes in TF-target relationships over physiological time scales. We tested this hypothesis using honey bee (Apis mellifera) division of labor as a model system by performing bioinformatic analyses of previously published brain transcriptomic profiles together with new RNAi and behavioral experiments. The bioinformatic analyses identified five TFs that exhibited strong signatures of regulatory plasticity as a function of division of labor. RNAi targeting of one of these TFs (broad complex) and a related TF that did not exhibit plasticity (fushi tarazu transcription factor 1) was administered in conjunction with automated analyses of foraging behavior in the field, laboratory assays of aggression and brood care behavior, and endocrine treatments. The results showed that changes in the regulatory relationships of these TFs were associated with behavioral state, social context and endocrine state. These findings provide the first empirical evidence that TF-target relationships in the brain are altered in conjunction with behavior and social context. They also suggest that one mechanism for this plasticity involves pleiotropic TFs high up in regulatory hierarchies producing behavior-specific transcriptional responses by activating different downstream TFs to induce discrete context-dependent transcriptional cascades. These findings provide new insights into the dynamic nature of the transcriptional regulatory architecture underlying behavior in the brain.

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Evolution of Nuclear Receptors in Insects

Cited by 18 publications

References 335 publications

How does juvenile hormone control insect metamorphosis and reproduction?

How does juvenile hormone control insect metamorphosis and reproduction?

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

Division of labor in honey bees is associated with transcriptional regulatory plasticity in the brain

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