Abstract
The neuronal and neuroendocrine peptides oxytocin (OT) and vasotocin (VT), including vasopressins, have six cognate receptors encoded by six receptor subtype genes in jawed vertebrates. The peptides elicit a broad range of responses that are specifically mediated by the receptor subtypes including neuronal functions regulating behavior and hormonal actions on reproduction and water/electrolyte balance. Previously, we have demonstrated that these six receptor subtype genes, which we designated VTR1A, VTR1B, OTR, VTR2A, VTR2B and VTR2C, arose from a syntenic ancestral gene pair, one VTR1/OTR ancestor and one VTR2 ancestor, through the early vertebrate whole-genome duplications (WGD) called 1R and 2R. This was supported by both phylogenetic and chromosomal conserved synteny data. More recently, other studies have focused on confounding factors, such as the OTR/VTR orthologs in cyclostomes, to question this scenario for the origin of the OTR/VTR gene family; proposing instead less parsimonious interpretations involving only one WGD followed by complex series of chromosomal or segmental duplications. Here, we have updated the phylogeny of the OTR/VTR gene family, including a larger number of vertebrate species, and revisited seven representative neighboring gene families from our previous conserved synteny analyses, adding chromosomal information from newer high-coverage genome assemblies from species that occupy key phylogenetic positions: the polypteriform fish reedfish (Erpetoichthys calabaricus), the cartilaginous fish thorny skate (Amblyraja radiata) and a more recent high-quality assembly of the Western clawed frog (Xenopus tropicalis) genome. Our analyses once again add strong support for four-fold symmetry, i.e., chromosome quadruplication in the same time window as the WGD events early in vertebrate evolution, prior to the jawed vertebrate radiation. Thus, the evolution of the OTR/VTR gene family can be most parsimoniously explained by two WGD events giving rise to the six ancestral genes, followed by differential gene losses of VTR2 genes in different lineages. We also argue for more coherence and clarity in the nomenclature of OT/VT receptors, based on the most parsimonious scenario.
Highlights
The two mammalian neuronal and neuroendocrine peptides oxytocin and vasopressin are involved in numerous functions, some of the most notable of which are reproduction and social behavior for oxytocin and water/electrolyte balance and social behavior for vasopressin [1]
We found that the reedfish genome contains the full ancestral jawed vertebrate complement of OT receptor (OTR)/VTR genes, and that these reedfish genes, in all cases but one, cluster in the expected positions in our phylogenies (Figures 1 and 2)
2.3.2 Elongated Intracellular Loop 3 in Teleost VTR2A We reported in a previous study [11] that teleost VTR2A genes seemed to have an elongated intracellular loop 3 (IL3)-encoding exon, producing a notably elongated middle portion of this intracellular loop
Summary
The two mammalian neuronal and neuroendocrine peptides oxytocin and vasopressin are involved in numerous functions, some of the most notable of which are reproduction and social behavior for oxytocin and water/electrolyte balance and social behavior for vasopressin [1]. As related peptides began to be isolated and characterized in the 1950s, including complete sequencing in several species, a tradition arose to give each new peptide with a unique sequence a distinct name [2] This resulted in a plethora of names, the most commonly used of which are isotocin (rayfinned fishes), mesotocin (non-eutherian tetrapods) and vasotocin (non-mammalian vertebrates). The most widespread vasopressin sequence in mammals was named argininevasopressin when it was discovered that the porcine sequence had replaced the arginine (Arg) residue on position 8 with lysine (Lys), lysine-vasopressin or lyspressin. This resulted in the abbreviation AVP for arginine-vasopressin. This naming mania arose long before it was possible to assign orthology between evolutionary lineages with certainty, and before the importance of orthology and paralogy for gene naming was realized
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