Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 13, 238

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

Affiliations

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

David Lagman et al. BMC Evol Biol.

Abstract

Background: Vertebrate 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).

Results: Sequence-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.

Conclusions: We 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.

Figures

Figure 1
Figure 1
Phylogenetic relationships between the visual opsin genes of the LWS, SWS1, SWS2, RH1 and RH2 clades. Tree topology inferred with the phylogenetic maximum likelihood method from an amino acid sequence alignment, supported by a non-parametric bootstrap analysis with 100 replicates. Red arrowheads indicate nodes with bootstrap values lower than 50% that were not considered informative. The tree is rooted with the human OPN3 sequence (not shown). Inlaid: (A) Neighbor joining (NJ) topology of the LWS clade, (B) NJ topology of the RH1 clade. See Additional file 2: Figures S1 and S2 for full trees, including all bootstrap values and root. For the sequence names, species abbreviations are applied as described in Methods, followed by the number of the chromosome or linkage group where the gene is located (if known) and the gene/subtype name (see Table 1). Scale bars indicate phylogenetic distance as number of substitutions per site.
Figure 2
Figure 2
Phylogenetic relationships between oxytocin and vasopressin receptor subtype genes. Tree topology inferred with the phylogenetic maximum likelihood method from an amino acid sequence alignment, supported by a non-parametric bootstrap analysis with 100 replicates. Arrowheads indicate nodes with bootstrap values lower than 50% that were not considered informative. Rooted with the common octopus OTR, CTR1 and CTR2 sequences (not shown). See Additional file 2: Figures S5 and S6 for full trees with all bootstrap values and root, including a neighbor joining topology. Sequence names and scale as in as in Figure 1. Teleost fish duplicates are indicated by brackets. The V2C sequences do not form a well-supported clade; this is also indicated with a bracket. Approved gene names are used for human, mouse and chicken genes, otherwise subtype names are used. Some of the sequence predictions used to make the tree are fragments and do not span the whole length of the alignment (see Additional file 1).
Figure 3
Figure 3
Conserved synteny between 2R-generated chromosome blocks. The identified paralogous chromosomal regions in the human, chicken and spotted gar genomes. In addition to the main gene families, the neighboring gene families with a full quartet of paralogous genes (ATP2B1, CAMK1, L1CAM and PLXNA) are included for reference. Colors are applied following the human and chicken chromosomes in order to show conserved synteny as well as sequence homology between species. Four paralogous regions can be observed in the human and spotted gar genomes. In the chicken genome the orthologs of the human genes on chromosome X could not be identified in the genome assembly. Orthologs for the genes on human chromosomes 7 and 12 are located on chromosome 1 in chicken and LG8 in spotted gar, indicating a split of this region in the human lineage. Several chicken genes have not been mapped to any chromosomal location. Their sequences for phylogenetic analyses were retrieved from NCBI. To facilitate comparisons between species, the names of the human orthologs have been applied to the chicken genes except for the visual opsin and OT/VP-R families where the gene names used in Figures 1 and 2 are applied. Note that the human and chicken V2 receptor sequences correspond to different subtypes: V2A and V2C respectively (Figure 2).
Figure 4
Figure 4
Paralogous chromosome blocks in the zebrafish genome. Gene families and colors applied as in Figure 3. Dashed boxes indicate divergences between the NJ tree and PhyML tree topologies. The color of the dashes nonetheless indicate the likely homology relationships. Orthologs of the human genes located on chromosomes 1, 3 and X are intermingled on zebrafish chromosomes 22, 8, 6, 11 and 23, indicating major rearrangements. In addition genes located on human chromosomes 7 and 12 and chicken chromosome 1 have orthologs on zebrafish chromosomes 25 and 4, indicating 3R-generated chromosome blocks. The black arrowhead marks the four local duplicates of the RH2 gene in the zebrafish genome (see Table 1). The full conserved synteny analysis, including all gene families and three-spined stickleback, is included in Additional file 5.
Figure 5
Figure 5
Proposed evolutionary history of the visual opsin gene-bearing chromosome regions. The proposed evolutionary scenario also includes the oxytocin/vasopressin receptor gene family (OT/VP-R), the voltage-gated calcium channel L-type alpha subunit gene family (CACNA1-L) and the G-protein alpha transducing (GNAT) and alpha inhibiting (GNAI) gene families. This scenario is consistent with data from additional neighboring gene families (see Conserved synteny analyses in Results). Local duplications before 2R occurred in the visual opsin and OT/VP-R gene families, giving rise to ancestral SWS and LWS genes, and ancestral V1/OTR and V2 genes respectively. The chromosome region subsequently quadrupled in 2R, giving rise to paralogous genes in all gene families. For the visual opsin gene family, the ancestral SWS gene gave rise to the SWS1, SWS2, RH1 and RH2 genes. However, only one copy of the LWS gene was retained. Early in actinopterygian evolution, before the divergence of spotted gar and teleost fishes, the RH1 gene was retrotransposed, giving rise to an intron-less RH1 duplicate. In the OT/VP-R family the V1B gene was lost. Following this, the chromosome regions duplicated in 3R, giving rise to duplicates of GNAI1, GNAI2, V1A, CACNA1D, CACNA1C and likely also RH1 (rho and rhol) and CACNA1F. We propose the nomenclature V1Aa and V1Ab for the 3R-generated V1A duplicates. After 3R, local duplications of the RH2, OTR and V2A genes occurred and extensive chromosomal rearrangements moved genes between the paralogous chromosome regions. Black arrowheads mark LWS, SWS1 and RH2 genes that have lineage-specific local duplicates in some teleost species.
Figure 6
Figure 6
Visual opsin gene repertoires in vertebrates. The tree to the left shows the evolutionary relationship between species used in our analyses, with the time-windows for the 2R and 3R events. The upper tree shows the relationship between LWS, SWS1, SWS2, RH1 and RH2 visual opsins inferred from phylogenetic analyses and synteny data. Black arrowheads mark the presence of local duplicates. The retrotransposition event that gave rise to intron-less rhodopsin (RH1) genes in spotted gar and teleosts is marked with a grey arrowhead in the left panel. The intron-less RH1 genes are called rho and rhol, and exorh denotes the exo-rhodopsin genes, using the approved zebrafish names. For human and zebrafish genes, the approved gene names are used as indicated in footnote a of Table 1.

Similar articles

See all similar articles

Cited by 35 PubMed Central articles

See all "Cited by" articles

References

    1. Hering L, Henze MJ, Kohler M, Kelber A, Bleidorn C, Leschke M, Nickel B, Meyer M, Kircher M, Sunnucks P, Mayer G. Opsins in onychophora (velvet worms) suggest a single origin and subsequent diversification of visual pigments in arthropods. Mol Biol Evol. 2012;29:3451–3458. doi: 10.1093/molbev/mss148. - DOI - PubMed
    1. Davies WIL, Collin SP, Hunt DM. Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol. 2012;21:3121–3158. doi: 10.1111/j.1365-294X.2012.05617.x. - DOI - PubMed
    1. Davies WL, Carvalho LS, Tay B-H, Brenner S, Hunt DM, Venkatesh B. Into the blue: gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant shark Callorhinchus milii. Genome Res. 2009;19:415–426. - PMC - PubMed
    1. Collin SP. Evolution and ecology of retinal photoreception in early vertebrates. Brain Behav Evol. 2010;75:174–185. doi: 10.1159/000314904. - DOI - PubMed
    1. Rennison DJ, Owens GL, Taylor JS. Opsin gene duplication and divergence in ray-finned fish. Mol Phylogenet Evol. 2012;62:986–1008. doi: 10.1016/j.ympev.2011.11.030. - DOI - PubMed

Publication types

LinkOut - more resources

Feedback