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      The Giant Mottled Eel, Anguilla marmorata, Uses Blue-Shifted Rod Photoreceptors during Upstream Migration

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          Abstract

          Catadromous fishes migrate between ocean and freshwater during particular phases of their life cycle. The dramatic environmental changes shape their physiological features, e.g. visual sensitivity, olfactory ability, and salinity tolerance. Anguilla marmorata, a catadromous eel, migrates upstream on dark nights, following the lunar cycle. Such behavior may be correlated with ontogenetic changes in sensory systems. Therefore, this study was designed to identify changes in spectral sensitivity and opsin gene expression of A. marmorata during upstream migration. Microspectrophotometry analysis revealed that the tropical eel possesses a duplex retina with rod and cone photoreceptors. The λ max of rod cells are 493, 489, and 489 nm in glass, yellow, and wild eels, while those of cone cells are 508, and 517 nm in yellow, and wild eels, respectively. Unlike European and American eels, Asian eels exhibited a blue-shifted pattern of rod photoreceptors during upstream migration. Quantitative gene expression analyses of four cloned opsin genes (Rh1f, Rh1d, Rh2, and SWS2) revealed that Rh1f expression is dominant at all three stages, while Rh1d is expressed only in older yellow eel. Furthermore, sequence comparison and protein modeling studies implied that a blue shift in Rh1d opsin may be induced by two known (N83, S292) and four putative (S124, V189, V286, I290) tuning sites adjacent to the retinal binding sites. Finally, expression of blue-shifted Rh1d opsin resulted in a spectral shift in rod photoreceptors. Our observations indicate that the giant mottled eel is color-blind, and its blue-shifted scotopic vision may influence its upstream migration behavior and habitat choice.

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          Most cited references39

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          Crystal structure of rhodopsin: A G protein-coupled receptor.

          Heterotrimeric guanine nucleotide-binding protein (G protein)-coupled receptors (GPCRs) respond to a variety of different external stimuli and activate G proteins. GPCRs share many structural features, including a bundle of seven transmembrane alpha helices connected by six loops of varying lengths. We determined the structure of rhodopsin from diffraction data extending to 2.8 angstroms resolution. The highly organized structure in the extracellular region, including a conserved disulfide bridge, forms a basis for the arrangement of the seven-helix transmembrane motif. The ground-state chromophore, 11-cis-retinal, holds the transmembrane region of the protein in the inactive conformation. Interactions of the chromophore with a cluster of key residues determine the wavelength of the maximum absorption. Changes in these interactions among rhodopsins facilitate color discrimination. Identification of a set of residues that mediate interactions between the transmembrane helices and the cytoplasmic surface, where G-protein activation occurs, also suggests a possible structural change upon photoactivation.
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            Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity.

            Phenotypic plasticity is the development of different phenotypes from a single genotype, depending on the environment. Such plasticity is a pervasive feature of life, is observed for various traits and is often argued to be the result of natural selection. A thorough study of phenotypic plasticity should thus include an ecological and an evolutionary perspective. Recent advances in large-scale gene expression technology make it possible to also study plasticity from a molecular perspective, and the addition of these data will help answer long-standing questions about this widespread phenomenon. In this review, we present examples of integrative studies that illustrate the molecular and cellular mechanisms underlying plastic traits, and show how new techniques will grow in importance in the study of these plastic molecular processes. These techniques include: (i) heterologous hybridization to DNA microarrays; (ii) next generation sequencing technologies applied to transcriptomics; (iii) techniques for studying the function of noncoding small RNAs; and (iv) proteomic tools. We also present recent studies on genetic model systems that uncover how environmental cues triggering different plastic responses are sensed and integrated by the organism. Finally, we describe recent work on changes in gene expression in response to an environmental cue that persist after the cue is removed. Such long-term responses are made possible by epigenetic molecular mechanisms, including DNA methylation. The results of these current studies help us outline future avenues for the study of plasticity.
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              In search of the visual pigment template.

              Absorbance spectra were recorded by microspectrophotometry from 39 different rod and cone types representing amphibians. reptiles, and fishes, with A1- or A2-based visual pigments and lambdamax ranging from 357 to 620 nm. The purpose was to investigate accuracy limits of putative universal templates for visual pigment absorbance spectra, and if possible to amend the templates to overcome the limitations. It was found that (1) the absorbance spectrum of frog rhodopsin extract very precisely parallels that of rod outer segments from the same individual, with only a slight hypsochromic shift in lambdamax, hence templates based on extracts are valid for absorbance in situ: (2) a template based on the bovine rhodopsin extract data of Partridge and De Grip (1991) describes the absorbance of amphibian rod outer segments excellently, contrary to recent electrophysiological results; (3) the lambdamax/lambda invariance of spectral shape fails for A1 pigments with small lambdamax and for A2 pigments with large lambdamax, but the deviations are systematic and can be readily incorporated into, for example, the Lamb (1995) template. We thus propose modified templates for the main "alpha-band" of A1 and A2 pigments and show that these describe both absorbance and spectral sensitivities of photoreceptors over the whole range of lambdamax. Subtraction of the alpha-band from the full absorbance spectrum leaves a "beta-band" described by a lambdamax-dependent Gaussian. We conclude that the idea of universal templates (one for A1- and one for A2-based visual pigments) remains valid and useful at the present level of accuracy of data on photoreceptor absorbance and sensitivity. The sum of our expressions for the alpha- and beta-band gives a good description for visual pigment spectra with lambdamax > 350 nm.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                7 August 2014
                : 9
                : 8
                : e103953
                Affiliations
                [1 ]Taiwan Ocean Research Institute, National Applied Research Laboratories, Kaohsiung, Taiwan
                [2 ]Sensory Physiology Laboratory, Marine Research Station, Academia Sinica, I-Lan County, Taiwan
                [3 ]Chemical Biology and Molecular Biophysics, Taiwan International Graduate Program, Institute of Biological Chemistry, Academia Sinica, Taipei, Taiwan
                [4 ]Institute of Biochemical Sciences, National Taiwan University, Taipei, Taiwan
                [5 ]Hanse-Wissenschaftskolleg Institute for Advanced Study, Delmenhorst, Germany
                [6 ]Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
                University of Florida, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: TYW FYW HYY. Performed the experiments: FYW WCF. Analyzed the data: FYW TYW ILW. Contributed reagents/materials/analysis tools: TYW HYY FYW. Wrote the paper: FYW TYW HYY.

                Article
                PONE-D-14-09887
                10.1371/journal.pone.0103953
                4125165
                25101636
                5abcc398-89a6-4d89-9e8c-ab86faec7a00
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 March 2014
                : 3 July 2014
                Page count
                Pages: 11
                Funding
                This study was supported by intramural grants from Academia Sinca, Taiwan, and by the National Science Council grants (NSC 100-2311-B-001-001-MY2, NSC 102-2311-B-001-019 and NSC 102-2311-B-001-010). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Fish Metamorphosis
                Ecology
                Behavioral Ecology
                Evolutionary Biology
                Evolutionary Genetics
                Evolutionary Physiology
                Marine Biology
                Fisheries Science
                Neuroscience
                Sensory Perception
                Vision
                Color Vision
                Sensory Systems
                Visual System
                Physiology
                Sensory Physiology
                Zoology
                Animal Behavior
                Animal Migration
                Homing Behavior
                Animal Physiology
                Vertebrate Physiology
                Fish Physiology
                Fish Biology

                Uncategorized
                Uncategorized

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