Multiple Kisspeptin Receptors in Early Osteichthyans Provide New Insights into the Evolution of This Receptor Family

International audienceDeorphanization of GPR54 receptor a decade ago led to the characterization of the kisspeptin receptor (Kissr) in mammalsand the discovery of its major role in the brain control of reproduction. While a single gene encodes for Kissr in eutherianmammals including human, other vertebrates present a variable number of Kissr genes, from none in birds, one or two inteleosts, to three in an amphibian, xenopus. In order to get more insight into the evolution of Kissr gene family, weinvestigated the presence of Kissr in osteichthyans of key-phylogenetical positions: the coelacanth, a representative of earlysarcopterygians, the spotted gar, a non-teleost actinopterygian, and the European eel, a member of an early group ofteleosts (elopomorphs). We report the occurrence of three Kissr for the first time in a teleost, the eel. As measured byquantitative RT-PCR, the three eel Kissr were differentially expressed in the brain-pituitary-gonadal axis, and differentiallyregulated in experimentally matured eels, as compared to prepubertal controls. Subfunctionalisation, as shown by thesedifferences in tissue distribution and regulation, may have represented significant evolutionary constraints for theconservation of multiple Kissr paralogs in this species. Furthermore, we identified four Kissr in both coelacanth and spottedgar genomes, providing the first evidence for the presence of four Kissr in vertebrates. Phylogenetic and syntenic analysessupported the existence of four Kissr paralogs in osteichthyans and allowed to propose a clarified nomenclature of Kissr(Kissr-1 to -4) based on these paralogs. Syntenic analysis suggested that the four Kissr paralogs arose through the tworounds of whole genome duplication (1R and 2R) in early vertebrates, followed by multiple gene loss events in theactinopterygian and sarcopterygian lineages. Due to gene loss there was no impact of the teleost-specific whole genomeduplication (3R) on the number of Kissr paralogs in current teleosts