Adaptation of cone pigments found in green rods for scotopic vision through a single amino acid mutation

Abstract

Most vertebrate retinas contain a single type of rod for scotopic vision and multiple types of cones for photopic and color vision. The retinas of certain amphibian species uniquely contain two types of rods: red rods, which express rhodopsin, and green rods, which express a blue-sensitive cone pigment (M1/SWS2 group). Spontaneous activation of rhodopsin induced by thermal isomerization of the retinal chromophore has been suggested to contribute to the rod's background noise, which limits the visual threshold for scotopic vision. Therefore, rhodopsin must exhibit low thermal isomerization rate compared with cone visual pigments to adapt to scotopic condition. In this study, we determined whether amphibian blue-sensitive cone pigments in green rods exhibit low thermal isomerization rates to act as rhodopsin-like pigments for scotopic vision. Anura blue-sensitive cone pigments exhibit low thermal isomerization rates similar to rhodopsin, whereas Urodela pigments exhibit high rates like other vertebrate cone pigments present in cones. Furthermore, by mutational analysis, we identified a key amino acid residue, Thr47, that is responsible for the low thermal isomerization rates of Anura blue-sensitive cone pigments. These results strongly suggest that, through this mutation, anurans acquired special blue-sensitive cone pigments in their green rods, which could form the molecular basis for scotopic color vision with normal red rods containing green-sensitive rhodopsin.photoreceptor cell | visual pigment | amphibian | molecular evolution | color discrimination

Pinopsin evolved as the ancestral dim-light visual opsin in vertebrates

“…Thus, we compared the thermal isomerization rates of the retinal chromophore between pinopsin and visual pigments. Recently, we developed a biochemical assay method to measure the thermal isomerization rate of the retinal chromophore of visual pigments 28 , 29 . Thermal isomerization rates ( k th ) are calculated using three experimentally determined values, namely v dark , v ligth , and k d (see details in Supplementary Figure 6A ).…”

“…The values of bovine rhodopsin, spotted gar rhodopsin, X. tropicalis pinopsin, and spotted gar pinopsin were calculated from the results shown in Supplementary Figure 6 . The values of X. tropicalis rhodopsin and three cone pigments were referred to our previous studies 28 , 29 . b Comparison of k th of rhodopsins, pinopsins, and cone pigments.…”

“…It has been reported that the active state of pinopsin decays more slowly than those of cone pigments, which can be accounted for by a loss of two amino acids in the second extracellular loop of pinopsin 43 . We previously revealed that there is a strong relationship between thermal isomerization rates of the retinal chromophore of visual pigments in the dark state and decay rates of the active state of the pigments 28 , 29 . Altogether, we speculate that a shortened second extracellular loop is also responsible for lower thermal isomerization rates of the retinal chromophore of pinopsin.…”

Vision using multiple distinct rod opsins in deep-sea fishes

“…Invertebrates are well documented to use differently tuned photoreceptors to enable colour discrimination in dim-light environments 32,33 . For vertebrates, only geckos and frogs have been shown to achieve a similar feat 34–36 . In these cases rod shaped photoreceptors rely on differently tuned cone visual pigments (e.g., in geckos 34 ) or a combination of cone pigments and a single rod photopigment (e.g., in frogs 35,36 ) to discriminate between colours.…”

“…For vertebrates, only geckos and frogs have been shown to achieve a similar feat 34–36 . In these cases rod shaped photoreceptors rely on differently tuned cone visual pigments (e.g., in geckos 34 ) or a combination of cone pigments and a single rod photopigment (e.g., in frogs 35,36 ) to discriminate between colours. Considering the relative simplicity of teleost brains, however, it is unlikely that D. argenteus is using colour opponency to compare between 14 differently tuned spectral channels.…”