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      Evolution of Retinoid and Steroid Signaling: Vertebrate Diversification from an Amphioxus Perspective

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          Abstract

          Although the physiological relevance of retinoids and steroids in vertebrates is very well established, the origin and evolution of the genetic machineries implicated in their metabolic pathways is still very poorly understood. We investigated the evolution of these genetic networks by conducting an exhaustive survey of components of the retinoid and steroid pathways in the genome of the invertebrate chordate amphioxus ( Branchiostoma floridae). Due to its phylogenetic position at the base of chordates, amphioxus is a very useful model to identify and study chordate versus vertebrate innovations, both on a morphological and a genomic level. We have characterized more than 220 amphioxus genes evolutionarily related to vertebrate components of the retinoid and steroid pathways and found that, globally, amphioxus has orthologs of most of the vertebrate components of these two pathways, with some very important exceptions. For example, we failed to identify a vertebrate-like machinery for retinoid storage, transport, and delivery in amphioxus and were also unable to characterize components of the adrenal steroid pathway in this invertebrate chordate. The absence of these genes from the amphioxus genome suggests that both an elaboration and a refinement of the retinoid and steroid pathways took place at the base of the vertebrate lineage. In stark contrast, we also identified massive amplifications in some amphioxus gene families, most extensively in the short-chain dehydrogenase/reductase superfamily, which, based on phylogenetic and genomic linkage analyses, were likely the result of duplications specific to the amphioxus lineage. In sum, this detailed characterization of genes implicated in retinoid and steroid signaling in amphioxus allows us not only to reconstruct an outline of these pathways in the ancestral chordate but also to discuss functional innovations in retinoid homeostasis and steroid-dependent regulation in both cephalochordate and vertebrate evolution.

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          Most cited references 147

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          The amphioxus genome and the evolution of the chordate karyotype.

          Lancelets ('amphioxus') are the modern survivors of an ancient chordate lineage, with a fossil record dating back to the Cambrian period. Here we describe the structure and gene content of the highly polymorphic approximately 520-megabase genome of the Florida lancelet Branchiostoma floridae, and analyse it in the context of chordate evolution. Whole-genome comparisons illuminate the murky relationships among the three chordate groups (tunicates, lancelets and vertebrates), and allow not only reconstruction of the gene complement of the last common chordate ancestor but also partial reconstruction of its genomic organization, as well as a description of two genome-wide duplications and subsequent reorganizations in the vertebrate lineage. These genome-scale events shaped the vertebrate genome and provided additional genetic variation for exploitation during vertebrate evolution.
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            The nuclear receptor superfamily: the second decade.

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              SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny.

              SEAVIEW and PHYLO_WIN are two graphic tools for X Windows-Unix computers dedicated to sequence alignment and molecular phylogenetics. SEAVIEW is a sequence alignment editor allowing manual or automatic alignment through an interface with CLUSTALW program. Alignment of large sequences with extensive length differences is made easier by a dot-plot-based routine. The PHYLO_WIN program allows phylogenetic tree building according to most usual methods (neighbor joining with numerous distance estimates, maximum parsimony, maximum likelihood), and a bootstrap analysis with any of them. Reconstructed trees can be drawn, edited, printed, stored, evaluated according to numerous criteria. Taxonomic species groups and sets of conserved regions can be defined by mouse and stored into sequence files, thus avoiding multiple data files. Both tools are entirely mouse driven. On-line help makes them easy to use. They are freely available by anonymous ftp at biom3.univ-lyon1.fr/pub/ mol_phylogeny or http:@acnuc.univ-lyon1.fr/, or by e-mail to galtier@biomserv.univ-lyon1.fr.
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                Author and article information

                Journal
                Genome Biol Evol
                gbe
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                2011
                18 August 2011
                2011
                18 August 2011
                : 3
                : 985-1005
                Affiliations
                [1 ]Departament de Genètica, Facultat de Biologia and Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Spain
                [2 ]Institut de Génomique Fonctionnelle de Lyon (UCBL, CNRS UMR5242, ENSL, INRA 1288), Ecole Normale Supérieure de Lyon, France
                Author notes
                [* ]Corresponding author: E-mail: ralbalat@ 123456ub.edu
                [†]

                These authors contributed equally to this work.

                Associate editor: Kateryna Makova

                Article
                10.1093/gbe/evr084
                3184775
                21856648
                The Author(s) 2011. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Research Article

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