Evolution of vertebrate GnRH receptors from the perspective of a Basal vertebrate

Abstract

This minireview provides the current status on gonadotropin-releasing hormone receptors (GnRH-R) in vertebrates, from the perspective of a basal vertebrate, the sea lamprey, and provides an evolutionary scheme based on the recent advance of whole genome sequencing. In addition, we provide a perspective on the functional divergence and evolution of the receptors. In this review we use the phylogenetic classification of vertebrate GnRH receptors that groups them into three clusters: type I (mammalian and non-mammalian), type II, and type III GnRH receptors. New findings show that the sea lamprey has two type III-like GnRH receptors and an ancestral type GnRH receptor that is more closely related to the type II-like receptors. These two novel GnRH receptors along with lGnRH-R-1 share similar structural features and amino acid motifs common to other known gnathostome type II/III receptors. Recent data analyses of the lamprey genome provide strong evidence that two whole rounds of genome duplication (2R) occurred prior to the gnathostome-agnathan split. Based on our current knowledge, it is proposed that lGnRH-R-1 evolved from an ancestor of the type II receptor following a vertebrate-shared genome duplication and that the two type III receptors resulted from a duplication within lamprey of a gene derived from a lineage shared by many vertebrates.

Keywords: G protein-coupled receptors; basal vertebrate; evolution; gonadotropin-releasing hormone receptors; hormone; lamprey; pituitary; receptor.

Figure 1

Gene structure of the three GnRH receptors in lamprey in the context of the current gene assembly. Exons are represented as black boxes with 5′- and 3′-UTRs in gray. In cases of incomplete data, angled-stippled fill is used for exons identified by cDNA sequencing that are not present among assembled scaffolds, and minimum lengths of the introns are provided based on the available flanking sequences of the scaffolds. Sf, Scaffold from Lamprey genome project consortium; details of the Ensembl scaffold designation are provided in parentheses, along with the size rounded to kilobase (kb). The position on the scaffold corresponding to the transcribed regions is below the boxes. At the bottom of each structure, the length of the deduced protein is given in amino acids with.

Figure 2

Working Hypothesis on the evolution of the GnRH receptor gene family in vertebrates with emphasis on placement of the lamprey genes. “D” represents duplication events for each of the 3 rounds of whole genome duplication in vertebrate evolution (1R, 2R, and 3R), the third being specific to teleosts. Open rectangles with red X’s indicate lost loci. Zebrafish are used here as a representative for teleosts. The half-shaded box for mammalian Type2 indicates that there is no functional gene product produced in several mammals, including humans. The cloud suggests the ambiguity concerning the relative time between early events, in particular the duration available for resolution of duplicated paralogs between the last common whole genome duplication event and the split of the agnathans from the gnathostome lineage. The dashed lines specify a proposed gene translocation, see Kim et al. (2011) for details and more vertebrates.