The vertebrate ancestral repertoire of visual opsins, transducin alpha subunits and oxytocin/vasopressin receptors was established by duplication of their shared genomic region in the two rounds of early vertebrate genome duplications

Abstract

BackgroundVertebrate color vision is dependent on four major color opsin subtypes: RH2 (green opsin), SWS1 (ultraviolet opsin), SWS2 (blue opsin), and LWS (red opsin). Together with the dim-light receptor rhodopsin (RH1), these form the family of vertebrate visual opsins. Vertebrate genomes contain many multi-membered gene families that can largely be explained by the two rounds of whole genome duplication (WGD) in the vertebrate ancestor (2R) followed by a third round in the teleost ancestor (3R). Related chromosome regions resulting from WGD or block duplications are said to form a paralogon. We describe here a paralogon containing the genes for visual opsins, the G-protein alpha subunit families for transducin (GNAT) and adenylyl cyclase inhibition (GNAI), the oxytocin and vasopressin receptors (OT/VP-R), and the L-type voltage-gated calcium channels (CACNA1-L).ResultsSequence-based phylogenies and analyses of conserved synteny show that the above-mentioned gene families, and many neighboring gene families, expanded in the early vertebrate WGDs. This allows us to deduce the following evolutionary scenario: The vertebrate ancestor had a chromosome containing the genes for two visual opsins, one GNAT, one GNAI, two OT/VP-Rs and one CACNA1-L gene. This chromosome was quadrupled in 2R. Subsequent gene losses resulted in a set of five visual opsin genes, three GNAT and GNAI genes, six OT/VP-R genes and four CACNA1-L genes. These regions were duplicated again in 3R resulting in additional teleost genes for some of the families. Major chromosomal rearrangements have taken place in the teleost genomes. By comparison with the corresponding chromosomal regions in the spotted gar, which diverged prior to 3R, we could time these rearrangements to post-3R.ConclusionsWe present an extensive analysis of the paralogon housing the visual opsin, GNAT and GNAI, OT/VP-R, and CACNA1-L gene families. The combined data imply that the early vertebrate WGD events contributed to the evolution of vision and the other neuronal and neuroendocrine functions exerted by the proteins encoded by these gene families. In pouched lamprey all five visual opsin genes have previously been identified, suggesting that lampreys diverged from the jawed vertebrates after 2R.

Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages

“…The chromosomal locations of the CRH family genes show that they are located in two distinct paralogons: CRH1, CRH2, and UCN1 reside in the same paralogon as the previously described opioid peptide and receptor genes (Dreborg et al 2008, Sundstrom et al 2010, Larhammar et al 2015, and the UCN2 and UCN3 genes are located in the paralogon harboring the visual opsin and oxytocin/ vasopressin receptor genes (Lagman et al 2013) (Fig. 3).…”

“…For each of the CRH family members, we also identified and analyzed gene families with members in the same chromosomal regions. This showed that the CRH family genes are located in two paralogons (sets of related chromosome regions), which have been previously analyzed in detail by us, namely the paralogon that contains the opioid peptide and receptor genes (Dreborg et al 2008, Sundstrom et al 2010, Larhammar et al 2015 and the one that contains the visual opsin genes and the oxytoc in and vasopressin receptor genes (Lagman et al 2013). This allowed us to distinguish orthologs and paralogs for the CRH family genes and to deduce that the CRH fami ly duplications took place as part of the basal vertebrate tetraploidizations (with one additional copy arising in the teleost tetraploidization, see below).…”

“…Taken together, the duplications of the two CRH subfamilies and the eight neighboring gene families (two of which consist of two subfamilies), as well as several additional gene families, located in these chromosomal regions (Dreborg et al 2008, Sundstrom et al 2010, Lagman et al 2013, Larhammar et al 2015 can most parsimoniously be explained by chromosome duplications (Fig. 3).…”

“…3). Each of these two paralogons has numerous other gene families represented on 2-4 of the chromosomes within each paralogon (Dreborg et al 2008, Sundstrom et al 2010, Lagman et al 2013, Larhammar et al 2015. Extensive conservation of gene synteny was found for several neighboring gene families in the genomes of human, chicken, and spotted gar.…”

“…Candidate genes were selected based on previous paralogon annotations of the opioid receptor and peptide genes (Sundstrom et al 2010, Larhammar et al 2015 and the visual opsin and oxytocin/vasopressin receptor genes (Lagman et al 2013). Orthologous genes were sought by querying the genome assemblies for the different species, and gene identity (ortholog vs paralog) was investigated by phylogenetic analyses following a similar procedure as described above for the CRH family members.…”