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      The Origins of Novel Protein Interactions during Animal Opsin Evolution

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      1 , 2 , 1 , *
      PLoS ONE
      Public Library of Science

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          Abstract

          Background

          Biologists are gaining an increased understanding of the genetic bases of phenotypic change during evolution. Nevertheless, the origins of phenotypes mediated by novel protein-protein interactions remain largely undocumented.

          Methodology/Principle Findings

          Here we analyze the evolution of opsin visual pigment proteins from the genomes of early branching animals, including a new class of opsins from Cnidaria. We combine these data with existing knowledge of the molecular basis of opsin function in a rigorous phylogenetic framework. We identify adaptive amino acid substitutions in duplicated opsin genes that correlate with a diversification of physiological pathways mediated by different protein-protein interactions.

          Conclusions/Significance

          This study documents how gene duplication events early in the history of animals followed by adaptive structural mutations increased organismal complexity by adding novel protein-protein interactions that underlie different physiological pathways. These pathways are central to vision and other photo-reactive phenotypes in most extant animals. Similar evolutionary processes may have been at work in generating other metazoan sensory systems and other physiological processes mediated by signal transduction.

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          Most cited references54

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          ProtTest: selection of best-fit models of protein evolution.

          Using an appropriate model of amino acid replacement is very important for the study of protein evolution and phylogenetic inference. We have built a tool for the selection of the best-fit model of evolution, among a set of candidate models, for a given protein sequence alignment. ProtTest is available under the GNU license from http://darwin.uvigo.es
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            Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea.

            A maximum likelihood method for inferring evolutionary trees from DNA sequence data was developed by Felsenstein (1981). In evaluating the extent to which the maximum likelihood tree is a significantly better representation of the true tree, it is important to estimate the variance of the difference between log likelihood of different tree topologies. Bootstrap resampling can be used for this purpose (Hasegawa et al. 1988; Hasegawa and Kishino 1989), but it imposes a great computation burden. To overcome this difficulty, we developed a new method for estimating the variance by expressing it explicitly. The method was applied to DNA sequence data from primates in order to evaluate the maximum likelihood branching order among Hominoidea. It was shown that, although the orangutan is convincingly placed as an outgroup of a human and African apes clade, the branching order among human, chimpanzee, and gorilla cannot be determined confidently from the DNA sequence data presently available when the evolutionary rate constancy is not assumed.
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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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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS ONE
                plos
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2007
                17 October 2007
                : 2
                : 10
                : e1054
                Affiliations
                [1 ]Ecology, Evolution and Marine Biology, University of California at Santa Barbara, Santa Barbara, California, United States of America
                [2 ]School of Integrative Biology, University of Queensland, Brisbane, Queensland, Australia
                Utrecht University, Netherlands
                Author notes
                * To whom correspondence should be addressed. E-mail: oakley@ 123456lifesci.ucsb.edu

                Conceived and designed the experiments: TO DP. Performed the experiments: TO DP. Analyzed the data: TO DP. Contributed reagents/materials/analysis tools: TO BD DP. Wrote the paper: TO BD DP.

                Article
                07-PONE-RA-01747R1
                10.1371/journal.pone.0001054
                2013938
                17940617
                79a0c0b0-ed33-4c07-9f49-08f699e172cb
                This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
                History
                : 12 July 2007
                : 17 September 2007
                Page count
                Pages: 9
                Categories
                Research Article
                Biochemistry/Bioinformatics
                Evolutionary Biology/Bioinformatics
                Evolutionary Biology/Evolutionary and Comparative Genetics

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                Uncategorized

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