Phototransduction and the Evolution of Photoreceptors

Photoreceptors in metazoans can be grouped into two classes, with their photoreceptive membrane derived either from cilia or microvilli. Both classes use some form of the visual pigment protein opsin, which together with 11-cis retinaldehyde absorbs light and activates a G-protein cascade, resulting in the opening or closing of ion channels. Considerable attention has recently been given to the molecular evolution of the opsins and other photoreceptor proteins; much is also known about transduction in the various photoreceptor types. Here we combine this knowledge in an attempt to understand why certain photoreceptors might have conferred particular selective advantages during evolution. We suggest that microvillar photoreceptors became predominant in most invertebrate species because of their single-photon sensitivity, high temporal resolution, and large dynamic range, and that rods and a duplex retina provided primitive chordates and vertebrates with similar sensitivity and dynamic range, but with a smaller expenditure of ATP.

[1]  J B Findlay,et al.  Isolation, Cloning, and Characterisation of a trp Homologue from Squid (Loligo forbesi) Photoreceptor Membranes , 1996, Journal of neurochemistry.

[2]  D. Stavenga Insect retinal pigments: Spectral characteristics and physiological functions , 1995, Progress in Retinal and Eye Research.

[3]  T. Wensel Signal transducing membrane complexes of photoreceptor outer segments , 2008, Vision Research.

[4]  Simon B. Laughlin,et al.  Visual ecology and voltage-gated ion channels in insect photoreceptors , 1995, Trends in Neurosciences.

[5]  A. Huber Scaffolding proteins organize multimolecular protein complexes for sensory signal transduction , 2001, The European journal of neuroscience.

[6]  D. Stavenga,et al.  Calcium Transients in the Rhabdomeres of Dark- and Light-Adapted Fly Photoreceptor Cells , 2000, The Journal of Neuroscience.

[7]  D. Hunt,et al.  Adaptive gene loss reflects differences in the visual ecology of basal vertebrates. , 2009, Molecular biology and evolution.

[8]  H. K. Hartline,et al.  The discharge of impulses in the optic nerve of Pecten in response to illumination of the eye , 1938 .

[9]  R. Hardie,et al.  Single photon responses in Drosophila photoreceptors and their regulation by Ca2+ , 2000, The Journal of physiology.

[10]  Hisao Tsukamoto,et al.  Cephalochordate Melanopsin: Evolutionary Linkage between Invertebrate Visual Cells and Vertebrate Photosensitive Retinal Ganglion Cells , 2005, Current Biology.

[11]  E. Nasi,et al.  A Direct Signaling Role for Phosphatidylinositol 4,5-Bisphosphate (PIP2) in the Visual Excitation Process of Microvillar Receptors* , 2005, Journal of Biological Chemistry.

[12]  Fred Rieke,et al.  Multiple Phosphorylation Sites Confer Reproducibility of the Rod's Single-Photon Responses , 2006, Science.

[13]  T. Lamb,et al.  Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup , 2007, Nature Reviews Neuroscience.

[14]  D. Nilsson,et al.  The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind , 2007, Journal of Comparative Physiology A.

[15]  Akihisa Terakita,et al.  The opsins , 2005, Genome Biology.

[16]  M. A. Knight,et al.  Ancient colour vision: multiple opsin genes in the ancestral vertebrates , 2003, Current Biology.

[17]  A. D. Blest The rapid synthesis and destruction of photoreceptor membrane by a dinopid spider: a daily cycle , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  Karin Pirhofer-Walzl,et al.  Adaptations for vision in dim light: impulse responses and bumps in nocturnal spider photoreceptor cells (Cupienniussalei Keys) , 2007, Journal of Comparative Physiology A.

[19]  B. Yoder,et al.  The Primary Cilium as a Complex Signaling Center , 2009, Current Biology.

[20]  Marten Postma,et al.  Mechanisms of Light Adaptation in Drosophila Photoreceptors , 2005, Current Biology.

[21]  Satoru Kawamura,et al.  Rod and cone photoreceptors: molecular basis of the difference in their physiology. , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[22]  J. Lisman,et al.  The excitation cascade of Limulus ventral photoreceptors: guanylate cyclase as the link between InsP3-mediated Ca2+ release and the opening of cGMP-gated channels , 2004, BMC Neuroscience.

[23]  Barbara Blakeslee,et al.  The intracellular pupil mechanism and photoreceptor signal: noise ratios in the fly Lucilia cuprina , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[24]  K. Yau,et al.  Phototransduction Motifs and Variations , 2009, Cell.

[25]  D. Arendt Evolution of eyes and photoreceptor cell types. , 2003, The International journal of developmental biology.

[26]  Marlies Dorlöchter,et al.  The Limulus ventral photoreceptor: Light response and the role of calcium in a classic preparation , 1997, Progress in Neurobiology.

[27]  V. Torre,et al.  Sensory Transduction , 1990, NATO ASI Series.

[28]  Juan M. Angueyra,et al.  Light-transduction in melanopsin-expressing photoreceptors of Amphioxus , 2009, Proceedings of the National Academy of Sciences.

[29]  Krzysztof Palczewski,et al.  Organization of the G Protein-coupled Receptors Rhodopsin and Opsin in Native Membranes* , 2003, Journal of Biological Chemistry.

[30]  María del Pilar Gomez,et al.  The light-sensitive conductance of hyperpolarizing invertebrate photoreceptors: a patch-clamp study , 1994, The Journal of general physiology.

[31]  Refractor Vision , 2000, The Lancet.

[32]  S. Laughlin,et al.  Temperature and the temporal resolving power of fly photoreceptors , 2000, Journal of Comparative Physiology A.

[33]  S. Laughlin,et al.  Fly Photoreceptors Demonstrate Energy-Information Trade-Offs in Neural Coding , 2007, PLoS biology.

[34]  W. Gehring,et al.  New perspectives on eye development and the evolution of eyes and photoreceptors. , 2005, The Journal of heredity.

[35]  K. Holmberg The hagfish retina: Electron microscopic study comparing receptor and epithelial cells in the pacific hagfish, Polistotrema stouti, with those in the atlantic hagfish, Myxine glutinosa , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[36]  F. Rieke,et al.  Recoverin Improves Rod-Mediated Vision by Enhancing Signal Transmission in the Mouse Retina , 2005, Neuron.

[37]  R. M. Eakin,et al.  Evolution of photoreceptors. , 1965, Cold Spring Harbor symposia on quantitative biology.

[38]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors: I. Response Dynamics and Signaling Efficiency at 25°C , 2001 .

[39]  S Conway Morris,et al.  The Cambrian "explosion": slow-fuse or megatonnage? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Current Biology , 2012, Current Biology.

[41]  A. Gorman,et al.  Photoreceptor Potentials of Opposite Polarity in the Eye of the Scallop, Pecten irradians , 1970, The Journal of general physiology.

[42]  K. Palczewski,et al.  Activation of rhodopsin: new insights from structural and biochemical studies. , 2001, Trends in biochemical sciences.

[43]  R. Weber,et al.  The Biology of Hagfishes , 1998, Springer Netherlands.

[44]  N. A. Locket,et al.  The Eyes of Hagfishes , 1998 .

[45]  R. Hardie,et al.  The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors , 1992, Neuron.

[46]  A. Gorman,et al.  Ionic effects on the membrane potential of hyperpolarizing photoreceptor in scallop retina , 1978, The Journal of physiology.

[47]  Dan-Eric Nilsson,et al.  The evolution of eyes and visually guided behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Cestmir Vlcek,et al.  Assembly of the cnidarian camera-type eye from vertebrate-like components , 2008, Proceedings of the National Academy of Sciences.

[49]  C. Montell,et al.  Phototransduction and retinal degeneration in Drosophila , 2007, Pflügers Archiv - European Journal of Physiology.

[50]  J. Dowling,et al.  Intracellular recordings from gecko photoreceptors during light and dark adaptation , 1975, The Journal of general physiology.

[51]  María del Pilar Gomez,et al.  Activation of light-dependent K+ channels in ciliary invertebrate photoreceptors involves cGMP but not the IP3/Ca2+ cascade , 1995, Neuron.

[52]  N. Artemyev,et al.  Unique transducins expressed in long and short photoreceptors of lamprey Petromyzon marinus , 2008, Vision Research.

[53]  M. Abs Physiology and behaviour of the pigeon , 1983 .

[54]  W. H. Miller,et al.  Comparative Physiology and Evolution of Vision in Invertebrates , 2011, Handbook of Sensory Physiology.

[55]  Thomas Cremer,et al.  Nuclear Architecture of Rod Photoreceptor Cells Adapts to Vision in Mammalian Evolution , 2009, Cell.

[56]  Alapakkam P Sampath,et al.  Optimization of single-photon response transmission at the rod-to-rod bipolar synapse. , 2007, Physiology.

[57]  V. Govardovskii,et al.  Visual cells and visual pigments of the lamprey,Lampetra fluviatilis , 1984, Journal of Comparative Physiology A.

[58]  H. Saibil,et al.  Ordered transmembrane and extracellular structure in squid photoreceptor microvilli , 1987, The Journal of cell biology.

[59]  F. Rieke,et al.  Nonlinear Signal Transfer from Mouse Rods to Bipolar Cells and Implications for Visual Sensitivity , 2002, Neuron.

[60]  R. Payne,et al.  Chapter 8 Phototransduction mechanisms in microvillar and ciliary photoreceptors of invertebrates , 2000 .

[61]  J. McInerney,et al.  Molecular evidence for dim-light vision in the last common ancestor of the vertebrates , 2006, Current Biology.

[62]  Eric J Warrant,et al.  Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps , 2008, Journal of Experimental Biology.

[63]  D. Baylor,et al.  Origin of reproducibility in the responses of retinal rods to single photons. , 1998, Biophysical journal.

[64]  R. Holmberg The hagfish retina: Fine structure of retinal cells in Myxine glutinosa, L., with special reference to receptor and epithelial cells , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[65]  G. Holmes,et al.  The sense organs , 1917 .

[66]  S B Laughlin,et al.  Intrinsic noise in locust photoreceptors. , 1982, The Journal of physiology.

[67]  María del Pilar Gomez,et al.  Light Transduction in Invertebrate Hyperpolarizing Photoreceptors: Possible Involvement of a Go-Regulated Guanylate Cyclase , 2000, The Journal of Neuroscience.

[68]  L. Kammermeier,et al.  The Sine oculis/Six class family of homeobox genes in jellyfish with and without eyes: development and eye regeneration. , 2004, Developmental biology.

[69]  Nicholas H. Putnam,et al.  The amphioxus genome illuminates vertebrate origins and cephalochordate biology. , 2008, Genome research.

[70]  S B Laughlin,et al.  Single photon signals in fly photoreceptors and first order interneurones at behavioral threshold. , 1981, The Journal of physiology.

[71]  R. Fernald Evolution of eyes , 2000, Current Opinion in Neurobiology.

[72]  K. Yau,et al.  Phototransduction in Rods and Cones , 2008 .

[73]  K. Hamdorf The Physiology of Invertebrate Visual Pigments , 1979 .

[74]  W. Gehring,et al.  Evolution and Functional Diversity of Jellyfish Opsins , 2008, Current Biology.

[75]  D. Arendt,et al.  Ciliary Photoreceptors with a Vertebrate-Type Opsin in an Invertebrate Brain , 2004, Science.

[76]  R. Hardie,et al.  Molecular Basis of Amplification in Drosophila Phototransduction Roles for G Protein, Phospholipase C, and Diacylglycerol Kinase , 2002, Neuron.

[77]  Voltage signal of photoreceptors at visual threshold , 1977, Nature.

[78]  Almut Kelber,et al.  A functional analysis of compound eye evolution. , 2007, Arthropod structure & development.

[79]  B. Walz,et al.  Structure and cellular physiology of Ca2+ stores in invertebrate photoreceptors. , 1995, Cell calcium.

[80]  Kosuke Takano,et al.  Jellyfish vision starts with cAMP signaling mediated by opsin-Gs cascade , 2008, Proceedings of the National Academy of Sciences.

[81]  T. Lacalli,et al.  Sensory Systems in Amphioxus: A Window on the Ancestral Chordate Condition , 2004, Brain, Behavior and Evolution.

[82]  A. Brodal,et al.  The biology of myxine , 1963 .

[83]  T. Lamb Evolution of vertebrate retinal photoreception , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[84]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[85]  B W Knight,et al.  Dispersion of latencies in photoreceptors of Limulus and the adapting- bump model , 1980, The Journal of general physiology.

[86]  D. Nilsson Eyes as optical alarm systems in fan worms and ark clams , 1994 .

[87]  Roger C. Hardie,et al.  Visual transduction in Drosophila , 2001, Nature.

[88]  D. Stavenga,et al.  Visual pigment spectra of the comma butterfly, Polygonia c-album, derived from in vivo epi-illumination microspectrophotometry , 2005, Journal of Comparative Physiology A.

[89]  F. Rieke,et al.  Mechanisms Regulating Variability of the Single Photon Responses of Mammalian Rod Photoreceptors , 2002, Neuron.

[90]  D. Tranchina,et al.  Multiple Steps of Phosphorylation of Activated Rhodopsin Can Account for the Reproducibility of Vertebrate Rod Single-photon Responses , 2003, The Journal of general physiology.

[91]  A. Gorman,et al.  Photoreceptors in Primitive Chordates: Fine Structure, Hyperpolarizing Receptor Potentials, and Evolution , 1971, Science.

[92]  Stuart N. Peirson,et al.  Melanopsin: an exciting photopigment , 2008, Trends in Neurosciences.

[93]  L. Salvini-Plawen Photoreception and the Polyphyletic Evolution of Photoreceptors (with Special Reference to Mollusca)* , 2008 .

[94]  R. Payne,et al.  Variants of TRP ion channel mRNA present in horseshoe crab ventral eye and brain , 2004, Journal of neurochemistry.

[95]  S. Laughlin Matching coding, circuits, cells, and molecules to signals: General principles of retinal design in the fly's eye , 1994, Progress in Retinal and Eye Research.

[96]  D. A. Burkhardt,et al.  Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[97]  E. Nasi Electrophysiological properties of isolated photoreceptors from the eye of Lima scabra , 1991, The Journal of general physiology.

[98]  K. Holmberg The Cyclostome Retina , 1977 .

[99]  Marten Postma,et al.  1.05 – Phototransduction in Microvillar Photoreceptors of Drosophila and Other Invertebrates , 2008 .

[100]  D. Nilsson,et al.  Visual Pigments: Trading Noise for Fast Recovery , 2004, Current Biology.

[101]  Gordon L. Fain,et al.  ATP Consumption by Mammalian Rod Photoreceptors in Darkness and in Light , 2008, Current Biology.

[102]  Karin Nordström,et al.  A simple visual system without neurons in jellyfish larvae , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[103]  B. Minke,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience Review Article Drosophila Photoreceptors and Signaling Mechanisms Structural and Optical Properties of the Diptera Compound Eye , 2022 .

[104]  M. Berridge,et al.  The versatility and universality of calcium signalling , 2000, Nature Reviews Molecular Cell Biology.