Abstract
Opn5 is a group within the opsin family of proteins that is responsible for visual and non-visual photoreception in animals. It consists of several subgroups, including Opn5m, the only subgroup containing members found in most vertebrates, including mammals. In addition, recent genomic information has revealed that some ray-finned fishes carry paralogous genes of Opn5m while other fishes have no such genes. Here, we report the molecular properties of the opsin now called Opn5m2 and its distributions in both the retina and brain. Like Opn5m, Opn5m2 exhibits UV light-sensitivity when binding to 11-cis-retinal and forms a stable active state that couples with Gi subtype of G protein. However, Opn5m2 does not bind all-trans-retinal and exhibits exclusive binding to 11-cis-retinal, whereas many bistable opsins, including fish Opn5m, can bind directly to all-trans-retinal as well as 11-cis-retinal. Because medaka fish has lost the Opn5m2 gene from its genome, we compared the tissue distribution patterns of Opn5m in medaka fish, zebrafish, and spotted gar, in addition to the distribution patterns of Opn5m2 in zebrafish and spotted gar. Opn5m expression levels showed a gradient along the dorsal–ventral axis of the retina, and preferential expression was observed in the ventral retina in the three fishes. The levels of Opn5m2 showed a similar gradient with preferential expression observed in the dorsal retina. Opn5m expression was relatively abundant in the inner region of the inner nuclear layer, while Opn5m2 was expressed in the outer edge of the inner nuclear layer. Additionally, we could detect Opn5m expression in several brain regions, including the hypothalamus, of these fish species. Opn5m2 expression could not be detected in zebrafish brain, but was clearly observed in limited brain regions of spotted gar. These results suggest that ray-finned fishes can generally utilize UV light information for non-image-forming photoreception in a wide range of cells in the retina and brain.
Highlights
Opsins constitute a photoreceptive G protein-coupled receptor family responsible for visual photoreception, such as image-forming and color vision, and for non-visual photoreception such as photoentrainment of circadian rhythm, photoperiodism, and pupillary light reflex in animals [1]
These opsins are expressed in retinal interneurons, including horizontal, bipolar, amacrine, and ganglion cells and multiple brain regions, which indicates that these opsins are responsible for non-image-forming photoreceptions
The other was found only in teleostei and holostei and constituted a sister group of Opn5m in the phylogenetic tree of Opn5 group (Fig 1)
Summary
Opsins constitute a photoreceptive G protein-coupled receptor family responsible for visual photoreception, such as image-forming and color vision, and for non-visual (nonimage-forming) photoreception such as photoentrainment of circadian rhythm, photoperiodism, and pupillary light reflex in animals [1]. Recent sequencing of vertebrate and invertebrate genomes has revealed that animals express diversified opsin genes in addition to visual pigments [3,4]. These opsins are expressed in retinal interneurons, including horizontal, bipolar, amacrine, and ganglion cells and multiple brain regions, which indicates that these opsins are responsible for non-image-forming photoreceptions. The analysis of its distribution patterns in birds and mammals revealed that Opn5m is localized to retinal interneurons, including the amacrine and ganglion cells, and several brain regions including the hypothalamus [8–11]. We characterized an additional Opn paralog found exclusively in ray-finned fishes that is closely related to Opn5m
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