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Rod and Cone Opsin Families Differ in Spectral Tuning Domains but Not Signal Transducing Domains as Judged by Saturated Evolutionary Trace Analysis

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Abstract

The visual receptor of rods and cones is a covalent complex of the apoprotein, opsin, and the light-sensitive chromophore, 11-cis-retinal. This pigment must fulfill many functions including photoactivation, spectral tuning, signal transmission, inactivation, and chromophore regeneration. Rod and cone photoreceptors employ distinct families of opsins. Although it is well known that these opsin families provide unique ranges in spectral sensitivity, it is unclear whether the families have additional functional differences. In this study, we use evolutionary trace (ET) analysis of 188 vertebrate opsin sequences to identify functionally important sites in each opsin family. We demonstrate the following results. (1) The available vertebrate opsin sequences produce a definitive description of all five vertebrate opsin families. This is the first demonstration of sequence saturation prior to ET analysis, which we term saturated ET (SET). (2) The cone opsin classes have class-specific sites compared to the rod opsin class. These sites reside in the transmembrane region and tune the spectral sensitivity of each opsin class to its characteristic wavelength range. (3) The cytoplasmic loops, primarily responsible for signal transmission and inactivation, are essentially invariant in rod versus cone opsins. This indicates that the electrophysiological differences between rod and cone photoreceptors cannot be ascribed to differences in the protein interaction regions of the opsins. SET shows that chromophore binding and regeneration are the only aspects of opsin structure likely to have functionally significant differences between rods and cones, whereas excitatory and adaptational properties of the opsin families appear to be functionally invariant.

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Acknowledgments

This work was supported by National Science Foundation Grant IBN-0131285 (to K.L.C), National Eye Institute Grant EY 05798 (to R.H.C.) and grants from the New Hampshire Agricultural Experiment Station. Thanks to Tom Kocher and two anonymous reviewers for comments on the manuscript. This is Scientific Contribution Number 2215 from the New Hampshire Agricultural Experiment Station.

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Authors and Affiliations

  1. Hubbard Center for Genome Studies, University of New Hampshire, Durham, NH, 03824, USA

    Karen L. Carleton & Tyrone C. Spady

  2. Department of Zoology, University of New Hampshire, Durham, NH, 03824, USA

    Karen L. Carleton & Tyrone C. Spady

  3. Department of Biochemistry and Molecular Biology, University of New Hampshire, Durham, NH, 03824, USA

    Rick H. Cote

  4. Hubbard Center for Genome Studies, University of New Hampshire, 438 Gregg Hall, 35 Colovos Road, Durham, NH, 03824, USA

    Karen L. Carleton

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  1. Karen L. Carleton
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Correspondence to Karen L. Carleton.

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Carleton, K.L., Spady, T.C. & Cote, R.H. Rod and Cone Opsin Families Differ in Spectral Tuning Domains but Not Signal Transducing Domains as Judged by Saturated Evolutionary Trace Analysis. J Mol Evol 61, 75–89 (2005). https://doi.org/10.1007/s00239-004-0289-z

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