Abstract

During the past decade, the kisspeptin system has been identified in various vertebrates, leading to the discovery of multiple genes encoding both peptides (Kiss) and receptors (Kissr). The investigation of recently published genomes from species of phylogenetic interest, such as a chondrichthyan, the elephant shark, an early sarcopterygian, the coelacanth, a non-teleost actinopterygian, the spotted gar, and an early teleost, the European eel, allowed us to get new insights into the molecular diversity and evolution of both Kiss and Kissr families. We identified four Kissr in the spotted gar and coelacanth genomes, providing the first evidence of four Kissr genes in vertebrates. We also found three Kiss in the coelacanth and elephant shark genomes revealing two new species, in addition to Xenopus, presenting three Kiss genes. Considering the increasing diversity of kisspeptin system, phylogenetic, and synteny analyses enabled us to clarify both Kiss and Kissr classifications. We also could trace back the evolution of both gene families from the early steps of vertebrate history. Four Kissr and four Kiss paralogs may have arisen via the two whole genome duplication rounds (1R and 2R) in early vertebrates. This would have been followed by multiple independent Kiss and Kissr gene losses in the sarcopterygian and actinopterygian lineages. In particular, no impact of the teleost-specific 3R could be recorded on the numbers of teleost Kissr or Kiss paralogs. The origin of their diversity via 1R and 2R, as well as the subsequent occurrence of multiple gene losses, represent common features of the evolutionary histories of Kiss and Kissr families in vertebrates. In contrast, comparisons also revealed un-matching numbers of Kiss and Kissr genes in some species, as well as a large variability of Kiss/Kissr couples according to species. These discrepancies support independent features of the Kiss and Kissr evolutionary histories across vertebrate radiation.

Highlights

  • As increasing vertebrate genomes have been explored, the understanding of their structure and evolution has progressed in parallel

  • Four Kissr and four Kiss paralogs may have arisen via the two whole genome duplication rounds (1R and 2R) in early vertebrates.This would have been followed by multiple independent Kiss and Kissr gene losses in the sarcopterygian and actinopterygian lineages

  • As one of the aims of this study was to compare the Kiss and Kissr histories, we first propose to make a short overview of our recent findings concerning the diversity, classification, and origin of Kissr gene family

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Summary

Introduction

As increasing vertebrate genomes have been explored, the understanding of their structure and evolution has progressed in parallel. The comparison of their gene organization shed light on various large-scale genomic events that occurred along vertebrate radiation Among those events, in the early stages of their history, vertebrates experienced two rounds of whole genome duplication (1R and 2R), resulting in fourfold-replicated genomes (Dehal and Boore, 2005; Van de Peer et al, 2010). In 2001, the orphan receptor GPR54 was identified as the cognate receptor of kisspeptin (Kotani et al, 2001; Muir et al, 2001) Two years later, both kisspeptin (Kiss) and its receptor (Kissr) were demonstrated as key players of the reproductive function in mammals (de Roux et al, 2003; Funes et al, 2003; Seminara et al, 2003).

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