Deep sequencing of the olfactory epithelium reveals specific chemosensory receptors are expressed at sexual maturity in the European eel Anguilla anguilla

Abstract

Vertebrate genomes encode a diversity of G protein-coupled receptor (GPCR) that belong to large gene families and are used by olfactory systems to detect chemical cues found in the environment. It is not clear however, if individual receptors from these large gene families have evolved roles that are specific to certain life stages. Here, we used deep sequencing to identify differentially expressed receptor transcripts in the olfactory epithelia (OE) of freshwater, seawater and sexually mature male eels (Anguilla anguilla). This species is particularly intriguing because of its complex life cycle, extreme long-distance migrations and early-branching position within the teleost phylogeny. In the A. anguillaOE, we identified full-length transcripts for 13, 112, 6 and 38 trace amine-associated receptors, odorant receptors (OR) and type I and type II vomeronasal receptors (V1R and V2R). Most of these receptors were expressed at similar levels at different life stages and a subset of OR and V2R-like transcripts was more abundant in sexually mature males suggesting that ORs and V2R-like genes are important for reproduction. We also identified a set of GPCR signal transduction genes that were differentially expressed indicating that eels make use of different GPCR signal transduction genes at different life stages. The finding that a diversity of chemosensory receptors is expressed in the olfactory epithelium and that a subset is differentially expressed suggests that most receptors belonging to large chemosensory gene families have functions that are important at multiple life stages, while a subset has evolved specific functions at different life stages.

Transcriptomic profiling of male European eel ( Anguilla anguilla ) livers at sexual maturity

“…In mammals, ABCA1 functions in cholesterol transport (Dean et al, 2001;Oram and Lawn, 2001) which is a precursor for bile acids. We confirmed that the ABCA1 transcript that was expressed at higher levels in immature males was distinct from those that were expressed at higher levels in sexually mature males by aligning them to two eel sequences from the A. anguilla olfactory transcriptome (Churcher et al, 2015). It therefore appears that the eel genome encodes multiple ABCA1 genes just like in zebrafish (Annilo et al, 2006).…”

Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals

“…Similarly, GPCRs can respond to diverse sensory ligands, including many odorants, light sensitive compounds, pheromones, and neurotransmitters (Brody and Cravchik 2000;Hewes and Taghert 2001). In line with other researchers, we assume that the levels of GPCR mRNAs give an indication of the activation of GPCR proteins (e.g., Churcher et al 2015;Thulasitha et al 2015;Quandt et al 2016), though it is also possible that GPCR genes could be transcriptionally activated by a pathway not involving the same GPCR. There was a strong and consistent profile of early up-regulation followed by later down-regulation and then dampening of expression, again consistent with the activation of alternative sensory modalities.…”

Trace Amines and Their Receptors

“…Similarly, clade III zebrafish TAARs have undergone strong positive selection (Hussain et al, 2009). Thus, the profiles of TAAR expression appear to be evolutionarily determined by adaptive responses; indeed, there is now evidence that TAAR expression can either be influenced by habitat changes or determine habitat choice (Churcher et al, 2015;Fatsini et al, 2016), consistent with a role in the detection and response to migratory cues.…”