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Adaptation of Cone Pigments Found in Green Rods for Scotopic Vision Through a Single Amino Acid Mutation

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Adaptation of Cone Pigments Found in Green Rods for Scotopic Vision Through a Single Amino Acid Mutation Adaptation of cone pigments found in green rods for scotopic vision through a single amino acid mutation Keiichi Kojimaa,1, Yuki Matsutania,1, Takahiro Yamashitaa, Masataka Yanagawab, Yasushi Imamotoa, Yumiko Yamanoc, Akimori Wadac, Osamu Hisatomid, Kanto Nishikawae, Keisuke Sakuraif, and Yoshinori Shichidaa,g,2 aDepartment of Biophysics, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan; bCellular Informatics Laboratory, RIKEN, Wako 351-0198, Japan; cDepartment of Organic Chemistry for Life Science, Kobe Pharmaceutical University, Kobe 658-8558, Japan; dDepartment of Earth and Space Science, Graduate School of Science, Osaka University, Osaka 560-0043, Japan; eGraduate School of Human and Environmental Studies, Kyoto University, Kyoto 606-8501, Japan; fFaculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8577, Japan; and gResearch Organization for Science and Technology, Ritsumeikan University, Kusatsu 525-8577, Japan Edited by King-Wai Yau, Johns Hopkins University School of Medicine, Baltimore, MD, and approved April 17, 2017 (received for review December 5, 2016) Most vertebrate retinas contain a single type of rod for scotopic order Gymnophiona are fossorial and have small eyes covered vision and multiple types of cones for photopic and color vision. with skin, which express only rhodopsin without cone pigments The retinas of certain amphibian species uniquely contain two (11). Moreover, amphibian species belonging to Anura and sev- types of rods: red rods, which express rhodopsin, and green rods, eral genera in Urodela, including Hynobius and Ambystoma,but which express a blue-sensitive cone pigment (M1/SWS2 group). neither Cynops nor Salamandra, are unique in possessing two Spontaneous activation of rhodopsin induced by thermal isomer- types of rods, red and green rods. Red rods are the normal rods ization of the retinal chromophore has been suggested to con- that express rhodopsin, whereas green rods express a blue- tribute to the rod’s background noise, which limits the visual sensitive cone pigment (12–16). Thus, our goal was to deter- threshold for scotopic vision. Therefore, rhodopsin must exhibit mine whether the blue-sensitive cone pigments in green rods ex- low thermal isomerization rate compared with cone visual pig- hibit molecular properties similar to that of rhodopsin or to that ments to adapt to scotopic condition. In this study, we determined of a typical cone pigment in cones. In this study, we compared the whether amphibian blue-sensitive cone pigments in green rods thermal isomerization rates of blue-sensitive cone pigments from exhibit low thermal isomerization rates to act as rhodopsin-like several amphibian species with those of rhodopsin and other cone BIOCHEMISTRY pigments for scotopic vision. Anura blue-sensitive cone pigments pigments. Our biochemical analysis revealed that Anura blue- exhibit low thermal isomerization rates similar to rhodopsin, sensitive cone pigments (Anura blues) acquired low thermal whereas Urodela pigments exhibit high rates like other vertebrate isomerization rates similar to rhodopsin through a single amino cone pigments present in cones. Furthermore, by mutational anal- acid mutation. We discuss the specialization process of blue- ysis, we identified a key amino acid residue, Thr47, that is respon- sensitive cone pigments in anuran green rods for scotopic vision. sible for the low thermal isomerization rates of Anura blue-sensitive cone pigments. These results strongly suggest that, through this Results and Discussion mutation, anurans acquired special blue-sensitive cone pigments Comparison of Thermal Isomerization Rates of Amphibian Blue- in their green rods, which could form the molecular basis for sco- Sensitive Cone Pigments. The thermal isomerization rates of the topic color vision with normal red rods containing green-sensitive retinal chromophore of visual pigments have been extensively rhodopsin. measured by electrophysiological analyses of photoreceptor photoreceptor cell | visual pigment | amphibian | molecular evolution | color discrimination Significance Anurans are unique in possessing two types of rod photore- ertebrate vision consists of scotopic and photopic vision, ceptor cells, red and green rods. Red rods express rhodopsin, triggered, respectively, by light absorption by the rod and V whereas green rods express blue-sensitive cone visual pig- cone photoreceptor cells of the retina (1). Scotopic vision re- ment. Rhodopsin exhibits a low rate of thermal isomerization quires high sensitivity and low threshold to be able to detect a of the retinal chromophore, which enables rods to detect few photons (2–4). Thus, electrical signals generated by single- photons with extremely high signal-to-noise for scotopic vi- photon absorptions in rods need to be reliably transmitted to sion. Here, we show that anuran blue-sensitive cone pigments higher-order retinal neurons in the presence of overwhelming acquired a rhodopsin-like property through a single amino acid intrinsic noise in rods, which is composed of two components: mutation at position 47 in the evolutionary process from other discrete and continuous noise (5). The former originates from cone pigments. Thus, anurans have special blue-sensitive cone thermal activation of the visual pigment, rhodopsin, and the pigments for the contribution of green rods to the low threshold latter results from spontaneous activation of the phosphodies- of light detection, which could form the molecular basis in tan- terase in the phototransduction cascade. Although the continuous dem with red rods containing rhodopsin in scotopic color vision. noise can be separated from the background noise, the discrete noise events are indistinguishable from true single-photon re- Author contributions: K.K., Y.M., T.Y., and Y.S. designed research; K.K. and Y.M. per- sponses (4, 6). Thus, the discrete noise sets a limit for the ab- formed research; M.Y., Y.I., Y.Y., A.W., O.H., K.N., and K.S. contributed new reagents/ solute visual threshold in scotopic vision (4, 7, 8). Thermal analytic tools; K.K., Y.M., T.Y., and Y.S. analyzed data; and K.K., T.Y., and Y.S. wrote activation of rhodopsin originates from the thermal isomeriza- the paper. tion of the retinal chromophore (9, 10). Taken together, sup- The authors declare no conflict of interest. pressing the thermal isomerization rates of the retinal in This article is a PNAS Direct Submission. rhodopsin improves the threshold of light detection. Data deposition: The sequences reported in this paper have been deposited in the GenBank Most vertebrates have one type of rod containing rhodopsin database (accession nos. LC180360, LC180361,andLC180362). and multiple types of cones containing different cone visual 1K.K. and Y.M. contributed equally to this work. pigments. Thus, they have the ability to discriminate color only 2To whom correspondence should be addressed. Email: [email protected]. under photopic conditions. By contrast, amphibians have diver- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. sified photoreceptor systems in their retinas. Most species in the 1073/pnas.1620010114/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1620010114 PNAS Early Edition | 1of6 Downloaded by guest on September 30, 2021 Fig. 1. Two-step reaction scheme of thermal activation and deactivation of visual pigments. R and R* indicate visual pigments in the inactive and active states, respectively. An opsin regenerated with normal 11-cis-retinal spontaneously converts to R* by thermal isomerization of retinal in the dark. After the first reaction, R* is degraded into opsin and retinal. cells from a series of genetically modified animals (17–19). that of rhodopsin in the course of molecular evolution after Recently, to better understand the molecular mechanism that anurans had acquired green rods. regulates the retinal thermal isomerization, we developed a Some urodelans also have green rods in their retina that biochemical method to estimate thermal isomerization rates by contain blue-sensitive cone pigments. Therefore, we determined using recombinant visual pigment proteins (10). Thermal isom- the thermal isomerization rates of blue-sensitive cone pigments erization rates (kth) are calculated using three experimentally from three urodelan species (Figs. S1−S3 and S4B). The tiger determined values in the following manner. First, we assumed a salamander (Ambystoma tigrinum) was reported to have green simplified two-step reaction as shown in Fig. 1, where R is the rods that express blue-sensitive cone pigments (14). The Mexican pigment in the inactive state and R* is the activated pigment by salamander (Ambystoma mexicanum) is a closely related species the thermal isomerization of the retinal chromophore. Given to the tiger salamander (23). The Japanese fire-bellied newt that the thermal isomerization occurs much slower than the (Cynops pyrrhogaster), however, has no green rods, and its blue- decay of R*(kth << kd), a steady-state approximation can be sensitive cone pigments are expressed only in blue cones (12). applied to the concentration of R*. (Here, kd is the spontaneous Our results show that the tiger salamander and Mexican sala- decay rate of the activated pigment.) Therefore, we obtain the mander blue-sensitive cone pigments (tiger salamander blue and following: Mexican salamander blue, respectively) exhibit thermal isomer- ization rates about 50-fold higher than that of bovine rhodopsin,
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