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      High opsin diversity in a non-visual infaunal brittle star

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          Abstract

          Background

          In metazoans, opsins are photosensitive proteins involved in both vision and non-visual photoreception. Echinoderms have no well-defined eyes but several opsin genes were found in the purple sea urchin ( Strongylocentrotus purpuratus) genome. Molecular data are lacking for other echinoderm classes although many species are known to be light sensitive.

          Results

          In this study focused on the European brittle star Amphiura filiformis, we first highlighted a blue-green light sensitivity using a behavioural approach. We then identified 13 new putative opsin genes against eight bona fide opsin genes in the genome of S. purpuratus. Six opsins were included in the rhabdomeric opsin group (r-opsins). In addition, one putative ciliary opsin (c-opsin), showing high similarity with the c-opsin of S. purpuratus (Sp-opsin 1), one Go opsin similar to Sp-opsins 3.1 and 3.2, two basal-branch opsins similar to Sp-opsins 2 and 5, and two neuropsins similar to Sp-opsin 8, were identified. Finally, two sequences from one putative RGR opsin similar to Sp-opsin 7 were also detected. Adult arm transcriptome analysis pinpointed opsin mRNAs corresponding to one r-opsin, one neuropsin and the homologue of Sp-opsin 2. Opsin phylogeny was determined by maximum likelihood and Bayesian analyses. Using antibodies designed against c- and r-opsins from S. purpuratus, we detected putative photoreceptor cells mainly in spines and tube feet of A. filiformis, respectively. The r-opsin expression pattern is similar to the one reported in S. purpuratus with cells labelled at the tip and at the base of the tube feet. In addition, r-opsin positive cells were also identified in the radial nerve of the arm. C-opsins positive cells, expressed in pedicellariae, spines, tube feet and epidermis in S. purpuratus were observed at the level of the spine stroma in the brittle star.

          Conclusion

          Light perception in A. filiformis seems to be mediated by opsins (c- and r-) in, at least, spines, tube feet and in the radial nerve cord. Other non-visual opsin types could participate to the light perception process indicating a complex expression pattern of opsins in this infaunal brittle star.

          Electronic supplementary material

          The online version of this article (doi:10.1186/1471-2164-15-1035) contains supplementary material, which is available to authorized users.

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          Most cited references132

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          Protein Identification and Analysis Tools on the ExPASy Server

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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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              Molecular tinkering of G protein-coupled receptors: an evolutionary success.

              Among membrane-bound receptors, the G protein-coupled receptors (GPCRs) are certainly the most diverse. They have been very successful during evolution, being capable of transducing messages as different as photons, organic odorants, nucleotides, nucleosides, peptides, lipids and proteins. Indirect studies, as well as two-dimensional crystallization of rhodopsin, have led to a useful model of a common 'central core', composed of seven transmembrane helical domains, and its structural modifications during activation. There are at least six families of GPCRs showing no sequence similarity. They use an amazing number of different domains both to bind their ligands and to activate G proteins. The fine-tuning of their coupling to G proteins is regulated by splicing, RNA editing and phosphorylation. Some GPCRs have been found to form either homo- or heterodimers with a structurally different GPCR, but also with membrane-bound proteins having one transmembrane domain such as nina-A, odr-4 or RAMP, the latter being involved in their targeting, function and pharmacology. Finally, some GPCRs are unfaithful to G proteins and interact directly, via their C-terminal domain, with proteins containing PDZ and Enabled/VASP homology (EVH)-like domains.
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                Author and article information

                Contributors
                jerome.delroisse@umons.ac.be
                estherullrich@gmx.de
                olga.ortega-martinez@bioenv.gu.se
                sam.dupont@bioenv.gu.se
                miarnone@szn.it
                jerome.mallefet@uclouvain.be
                patrick.flammang@umons.ac.be
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                28 November 2014
                2014
                : 15
                : 1
                : 1035
                Affiliations
                [ ]Biology of Marine Organisms and Biomimetics, Research Institute for Biosciences, University of Mons, Avenue du Champs de Mars 6, 7000 Mons, Belgium
                [ ]Museum für Naturkunde, Invalidenstr. 43, 10115 Berlin, Germany
                [ ]Department of Biological and Environmental Science, The Sven Lovén Centre for Marine Sciences – Kristineberg, University of Gothenburg, 45178 Fiskebäckskil, Sweden
                [ ]Stazione Zoologica Anton Dohrn, Cellular and Developmental Biology, Villa Comunale, 80121 Naples, Italy
                [ ]Laboratory of Marine Biology, Earth and Life Institute, Catholic University of Louvain, Louvain-La-Neuve, Place Croix du Sud 3, bt L7.06.04, 1348 Louvain-la-Neuve, Belgium
                Article
                6862
                10.1186/1471-2164-15-1035
                4289182
                25429842
                6e804527-6799-431e-b092-7215c6f3a7a2
                © Delroisse et al.; licensee BioMed Central. 2014

                This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 22 July 2014
                : 19 November 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                opsin,echinodermata,ophiuroidea,photoreception,genome,transcriptome
                Genetics
                opsin, echinodermata, ophiuroidea, photoreception, genome, transcriptome

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