Retinoid X receptor modulates olfactory attraction through Gα signaling in the migratory locusts

Animals communicate with each other in aggregating for survival and adaptation. Solitary locusts show an olfactory transition from repulsion to attraction in aggregation. However, the molecular mechanism underlying this transition is less well known. In this study, we explored differentially expressed transcripts (DETs) during locust aggregation and identified that a functional class of general metabolism encompassed the largest number of DETs among all analyzed gene classes. Within this functional class of general metabolism, oxidoreductase mediates synthesis of retinoic acid (RA) from vitamin A and other metabolites derived from carbohydrates. The expression levels of retinaldehyde hydroxylase 1 (raldh1) and retinoid X receptor (rxr), which are two crucial genes for RA synthesis and signaling, were upregulated during 4 h of crowding. Knockdown of raldh1 and rxr by RNA interference (RNAi) in the brains resulted in the loss of olfactory attraction. Moreover, inhibition of RXR by RNAi resulted in downregulated expression of Gna14, a member of the Gα subfamily that transduces signals in G protein-coupled receptor (GPCR) pathways. Abrogating RXR signaling and Gna14 by RNAi knockdown inhibited the function of dopamine receptor 1 (DopR1) and octopamine receptor α1 (OctαR1) in modulating olfactory attraction. RXR signaling is essential for DopR1 and OctαR1 to mediate olfactory attraction. This study showed that RXR signaling mediates attraction by Gα signaling and confirmed a novel link between nuclear receptor RXR and the membrane receptor GPCRs in modulating olfactory attraction.