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Genes Genet Syst
2019 Oct 30;944:141-149. doi: 10.1266/ggs.19-00009.
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Evolution of V1R pheromone receptor genes in vertebrates: diversity and commonality.
Nikaido M
.
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The vomeronasal organ (VNO) plays a key role in sensing pheromonal cues, which elicit innate responses and induce social and sexual behaviors. The vomeronasal receptor 1 genes, V1Rs, encode members of a pheromone receptor family that are mainly expressed in the VNO. Previous studies have revealed that the V1R family shows extraordinary variety among mammalian species owing to successive gene gains and losses. Because species-specific pheromonal interaction may facilitate species-specific reproductive behaviors, understanding the evolution of V1Rs in terms of their origin, repertoire and phylogeny should provide insight into the mechanisms of animal diversification. Here I summarize recent studies about the V1R family from its initial discovery in the rat genome to extensive comparative analyses among vertebrates. I further introduce our recent findings for V1Rs in a broad range of vertebrates, which reveal unexpected diversity as well as shared features common among lineages.
Fig. 1.
Schematic diagram of the mammalian olfactory system highlighting the VNO. Sagittal view of a mouse head showing the main olfactory epithelium (MOE), vomeronasal organ (VNO), main olfactory bulb (MOB) and accessory olfactory bulb (AOB). A coronal view of the VNO is shown in the box. In the VNO, apical VSNs express V1Rs and project their axons to the anterior (red) AOB, and basal VSNs express V2Rs and project to the posterior (yellow) AOB.
Fig. 2.
Number of intact V1Rs among a broad range of vertebrates. In the graph on the right, bars for species having more than 100 gene copies are truncated and the actual numbers are indicated. The phylogenetic tree of vertebrates with taxonomic classification names is shown on the left side. The copy number was based on the following references (Saraiva and Korsching, 2007; Date-Ito et al., 2008; Grus and Zhang, 2009; Young et al., 2010; Ota et al., 2012; Nikaido et al., 2013; Zapilko and Korsching, 2016; Moriya-Ito et al., 2018). Note that the V1R repertoire is highly variable in mammals, from 283 in platypus to 0 in dolphin and bat, but much less variable in teleost fish (6 copies in most species). The number of V1Rs increases dramatically in species belonging to the Sarcopterygii.
Fig. 3.
Evolutionary relationships of t-V1Rs, f-V1Rs and ancV1R. The maximum likelihood tree of the amino acid sequences of V1Rs of 10 representative vertebrates under the JTT+G+F model constructed by RAxML 8.2.4 (Guindon and Gascuel, 2003). The scale bar indicates amino acid substitutions per site. The species are indicated as follows: cow (gray), frog (green), coelacanth (red), five teleost fishes – zebrafish, stickleback, fugu, pufferfish and medaka – (blue), elephant shark (hash #), sea lamprey (star *). The bitter taste receptor type 2 sequences of vertebrates were used for outgroups of V1Rs. Note that the f-V1Rs originated earlier than t-V1Rs, which are derived from the common ancestor of f-V1R1 and f-V1R2. Importantly, an orthologous relationship is shared among a broad range of species including cow, frog and coelacanth for ancV1R but not for t-V1Rs or f-V1Rs. Recently, ancV1R was shown to be shared among most bony vertebrates (Suzuki et al., 2018).
Fig. 4.
(A) Evolutionary scenario of ancV1R during vertebrate evolution. ancV1R emerged in the common ancestor of Sarcopterygii and Actinopterygii more than 400 million years ago and was lost in each of the common ancestors (gray circles) of teleost fishes as well as turtles, alligators and birds (gray dashed lines and silhouettes) by pseudogenization. The white silhouette and dashed black lines associated with sharks indicate that ancV1R has not yet emerged. Figure adapted from Suzuki et al. (2018). (B) Distinct pattern of expression between canonical VRs and ancV1R in the VNO. In situ hybridization on coronal sections of the VNO of C57BL/6 mice was performed using probes against canonical V1R (V1Rh5, left) and V2R (V2Ra, middle), and ancV1R (right). Note that canonical V1R and V2R show punctate expression in the apical and basal regions of the vomeronasal epithelium, respectively, according to the one neuron–one receptor rule. However, ancV1R shows broad expression in most vomeronasal sensory neurons, suggesting a new “one neuron–two receptors” (canonical V1R or V2R + ancV1R) rule. Scale bar indicates 200 μm.
