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      Insights into bilaterian evolution from three spiralian genomes

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          Abstract

          Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ecologically and as experimental systems in classical embryology 13 . Here we describe the draft genomes of the owl limpet ( Lottia gigantea), a marine polychaete ( Capitella teleta) and a freshwater leech ( Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversification of bilaterians from a genomic perspective. We find that the genome organization, gene structure and functional content of these species are more similar to those of some invertebrate deuterostome genomes (for example, amphioxus and sea urchin) than those of other protostomes that have been sequenced to date (flies, nematodes and flatworms). The conservation of these genomic features enables us to expand the inventory of genes present in the last common bilaterian ancestor, establish the tripartite diversification of bilaterians using multiple genomic characteristics and identify ancient conserved long- and short-range genetic linkages across metazoans. Superimposed on this broadly conserved pan-bilaterian background we find examples of lineage-specific genome evolution, including varying rates of rearrangement, intron gain and loss, expansions and contractions of gene families, and the evolution of clade-specific genes that produce the unique content of each genome.

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          Most cited references21

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          Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

          Sea anemones are seemingly primitive animals that, along with corals, jellyfish, and hydras, constitute the oldest eumetazoan phylum, the Cnidaria. Here, we report a comparative analysis of the draft genome of an emerging cnidarian model, the starlet sea anemone Nematostella vectensis. The sea anemone genome is complex, with a gene repertoire, exon-intron structure, and large-scale gene linkage more similar to vertebrates than to flies or nematodes, implying that the genome of the eumetazoan ancestor was similarly complex. Nearly one-fifth of the inferred genes of the ancestor are eumetazoan novelties, which are enriched for animal functions like cell signaling, adhesion, and synaptic transmission. Analysis of diverse pathways suggests that these gene "inventions" along the lineage leading to animals were likely already well integrated with preexisting eukaryotic genes in the eumetazoan progenitor.
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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 Amphimedon queenslandica genome and the evolution of animal complexity.

              Sponges are an ancient group of animals that diverged from other metazoans over 600 million years ago. Here we present the draft genome sequence of Amphimedon queenslandica, a demosponge from the Great Barrier Reef, and show that it is remarkably similar to other animal genomes in content, structure and organization. Comparative analysis enabled by the sequencing of the sponge genome reveals genomic events linked to the origin and early evolution of animals, including the appearance, expansion and diversification of pan-metazoan transcription factor, signalling pathway and structural genes. This diverse 'toolkit' of genes correlates with critical aspects of all metazoan body plans, and comprises cell cycle control and growth, development, somatic- and germ-cell specification, cell adhesion, innate immunity and allorecognition. Notably, many of the genes associated with the emergence of animals are also implicated in cancer, which arises from defects in basic processes associated with metazoan multicellularity.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                21 May 2014
                19 December 2012
                24 January 2013
                07 July 2014
                : 493
                : 7433
                : 526-531
                Affiliations
                [1 ]European Molecular Biology Laboratory, Meyerhofstraße 1, 69117 Heidelberg, Germany
                [2 ]Department of Molecular and Cell Biology, University of California, Berkeley, California 94720, USA
                [3 ]Department of Ecology & Evolutionary Biology, Rice University, PO Box 1892, Houston, Texas 77251-1892, USA
                [4 ]DOE Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California 94598, USA
                [5 ]Department of Biology, Williams College, Thompson Biology Laboratory, 59 Lab Campus Drive, Williamstown, Massachusetts 01267, USA
                [6 ]Children’s Hospital Oakland Research Institute, 5700 Martin Luther King Jr. Way, Oakland, California 94609, USA
                [7 ]Hudson Alpha Institute for Biotechnology, 601 Genome Way, Huntsville, Alabama 35806-2908, USA
                [8 ]Department of Integrative Biology, University of California, Berkeley, California 94720, USA
                [9 ]Kewalo Marine Laboratory, University of Hawaii at Manoa, 41 Ahui Street, Honolulu, Hawaii 96813, USA
                [10 ]Department of Biochemistry and Cell Biology, Rice University, Houston, Texas 77251, USA
                [11 ]Okinawa Institute of Science and Technology, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan
                Author notes
                Correspondence and requests for materials should be addressed to N.H.P. ( nputnam@ 123456gmail.com ) or D.S.R. ( dsrokhsar@ 123456gmail.com )
                [†]

                Present addresses: Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK (F.M.); Insitute of Zoology, National Taiwan University, 1 Roosevelt Road, Taipei 10617, Taiwan (D.-H.K.); Genome Project Solutions, 1024 Promenade Street, Hercules, California 94547, USA (J.L.B.); The Whitney Laboratory for Marine Bioscience, 9505 Ocean Shore Boulevard, St. Augustine, Florida 32080-8610, USA (E.C.S.).

                Article
                NIHMS587989
                10.1038/nature11696
                4085046
                23254933
                3fd8bfff-1575-4081-b624-18ed3e7245d5
                © 2013 Macmillan Publishers Limited. All rights reserved

                This work is licensed under a Creative Commons Attribution-NonCommercial-Share Alike 3.0 Unported licence. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-sa/3.0

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