title: An extended family of novel vertebrate photopigments is widely expressed and displays a diversity of function.
abstract: Light affects animal physiology and behavior more than simply through classical visual, image-forming pathways. Nonvisual photoreception regulates numerous biological systems, including circadian entrainment, DNA repair, metabolism, and behavior. However, for the majority of these processes, the photoreceptive molecules involved are unknown. Given the diversity of photophysiological responses, the question arises whether a single photopigment or a greater diversity of proteins within the opsin superfamily detect photic stimuli. Here, a functional genomics approach identified the full complement of photopigments in a highly light-sensitive model vertebrate, the zebrafish (Danio rerio), and characterized their tissue distribution, expression levels, and biochemical properties. The results presented here reveal the presence of 42 distinct genes encoding 10 classical visual photopigments and 32 nonvisual opsins, including 10 novel opsin genes comprising four new pigment classes. Consistent with the presence of light-entrainable circadian oscillators in zebrafish, all adult tissues examined expressed two or more opsins, including several novel opsins. Spectral and electrophysiological analyses of the new opsins demonstrate that they form functional photopigments, each with unique chromophore-binding and wavelength specificities. This study has revealed a remarkable number and diversity of photopigments in zebrafish, the largest number so far discovered for any vertebrate. Found in amphibians, reptiles, birds, and all three mammalian clades, most of these genes are not restricted to teleosts. Therefore, nonvisual light detection is far more complex than initially appreciated, which has significant biological implications in understanding photoreception in vertebrates.
authors.affiliation: School of Animal Biology and University of Western Australia Oceans Institute, University of Western Australia, Perth, Western Australia 6009, Australia; Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, OX3 9DU, United Kingdom;
authors.forename: Wayne I L
authors.initials: WI
authors.lastname: Davies
authors.affiliation: Centre for Cell and Molecular Dynamics, Department of Cell and Developmental Biology, University College London, London, WC1E 6DE, United Kingdom;
authors.forename: T Katherine
authors.initials: TK
authors.lastname: Tamai
authors.affiliation: Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, OX3 9DU, United Kingdom;
authors.forename: Lei
authors.initials: L
authors.lastname: Zheng
authors.affiliation: Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, OX3 9DU, United Kingdom;
authors.forename: Josephine K
authors.initials: JK
authors.lastname: Fu
authors.affiliation: Department of Cell and Developmental Biology, University College London, London, WC1E 6BT, United Kingdom.
authors.forename: Jason
authors.initials: J
authors.lastname: Rihel
authors.affiliation: Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, OX3 9DU, United Kingdom;
authors.forename: Russell G
authors.initials: RG
authors.lastname: Foster
authors.affiliation: Centre for Cell and Molecular Dynamics, Department of Cell and Developmental Biology, University College London, London, WC1E 6DE, United Kingdom;
authors.forename: David
authors.initials: D
authors.lastname: Whitmore
authors.affiliation: Nuffield Laboratory of Ophthalmology, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, OX3 9DU, United Kingdom;
authors.forename: Mark W
authors.initials: MW
authors.lastname: Hankins
mesh_terms: D000663:Amphibians / Q000235:genetics; D000818:Animals; D001717:Birds / Q000235:genetics; D019143:Evolution, Molecular; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation; D016678:Genome; D023281:Genomics; D008027:Light; D008322:Mammals / Q000235:genetics; D055355:Opsins / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015027:Zebrafish / Q000235:genetics*
chemical_list: D055355:Opsins; D012333:RNA, Messenger