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      The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

      research-article

      1 , 2 , 3 , 4 , 5 , 6 , 1 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 13 , 1 , 14 , 14 , 14 , 14 , 15 , 16 , 13 , 2 , 1 , 17 , 18 , 14 , 5 , 19 , 1 , 9 , 14 , 20 , 14 , 21 , 14 , 14 , 22 , 1 , 14 , 18 , 8 , 1 , 23 , 8 , 8 , 13 , 24 , 25 , 26 , 14 , , 27 , , 14 , , 17 , , 10 , 28 , , 7 , , 4 , , 8 , , 29 , , 8 , , 14 , , 1

      BMC Biology

      BioMed Central

      Parasteatoda tepidariorum, Genome, Centruroides sculpturatus, Gene duplication, Evolution, Hox genes

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          Abstract

          Background

          The duplication of genes can occur through various mechanisms and is thought to make a major contribution to the evolutionary diversification of organisms. There is increasing evidence for a large-scale duplication of genes in some chelicerate lineages including two rounds of whole genome duplication (WGD) in horseshoe crabs. To investigate this further, we sequenced and analyzed the genome of the common house spider Parasteatoda tepidariorum.

          Results

          We found pervasive duplication of both coding and non-coding genes in this spider, including two clusters of Hox genes. Analysis of synteny conservation across the P. tepidariorum genome suggests that there has been an ancient WGD in spiders. Comparison with the genomes of other chelicerates, including that of the newly sequenced bark scorpion Centruroides sculpturatus, suggests that this event occurred in the common ancestor of spiders and scorpions, and is probably independent of the WGDs in horseshoe crabs. Furthermore, characterization of the sequence and expression of the Hox paralogs in P. tepidariorum suggests that many have been subject to neo-functionalization and/or sub-functionalization since their duplication.

          Conclusions

          Our results reveal that spiders and scorpions are likely the descendants of a polyploid ancestor that lived more than 450 MYA. Given the extensive morphological diversity and ecological adaptations found among these animals, rivaling those of vertebrates, our study of the ancient WGD event in Arachnopulmonata provides a new comparative platform to explore common and divergent evolutionary outcomes of polyploidization events across eukaryotes.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12915-017-0399-x) contains supplementary material, which is available to authorized users.

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          Most cited references 86

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          Activities at the Universal Protein Resource (UniProt)

          The mission of the Universal Protein Resource (UniProt) (http://www.uniprot.org) is to provide the scientific community with a comprehensive, high-quality and freely accessible resource of protein sequences and functional annotation. It integrates, interprets and standardizes data from literature and numerous resources to achieve the most comprehensive catalog possible of protein information. The central activities are the biocuration of the UniProt Knowledgebase and the dissemination of these data through our Web site and web services. UniProt is produced by the UniProt Consortium, which consists of groups from the European Bioinformatics Institute (EBI), the SIB Swiss Institute of Bioinformatics (SIB) and the Protein Information Resource (PIR). UniProt is updated and distributed every 4 weeks and can be accessed online for searches or downloads.
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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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              Streaming fragment assignment for real-time analysis of sequencing experiments

              We present eXpress, a software package for highly efficient probabilistic assignment of ambiguously mapping sequenced fragments. eXpress uses a streaming algorithm with linear run time and constant memory use. It can determine abundances of sequenced molecules in real time, and can be applied to ChIP-seq, metagenomics and other large-scale sequencing data. We demonstrate its use on RNA-seq data, showing greater efficiency than other quantification methods.
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                Author and article information

                Contributors
                evelyn_schwager@uml.edu
                prashant.sharma@wisc.edu
                toby.h.clarke@gmail.com
                danielleite@brookes.ac.uk
                torsten.wierschin@gmail.com
                pechmanm@uni-koeln.de
                yasuko@brh.co.jp
                espositola@gmail.com
                jesper.bechsgaard@bios.au.dk
                trine.bilde@bios.au.dk
                alex.buffry-2015@brookes.ac.uk
                hchao@bcm.edu
                hdinh@bcm.edu
                doddapan@bcm.edu
                sdugan@bcm.edu
                cornelius.eibner@uni-jena.de
                extavour@oeb.harvard.edu
                peter.funch@biology.au.dk
                jessica_garb@uml.edu
                luis.baudouin.gonzalez-2016@brookes.ac.uk
                gonzalezv@si.edu
                sam.griffiths-jones@manchester.ac.uk
                yhan@bcm.edu
                cheryl.hayashi@ucr.edu
                m.hilbrant@uni-koeln.de
                dsthughes@gmail.com
                ralf.janssen@geo.uu.se
                sllee@bcm.edu
                nacho.maeso@gmail.com
                shwethacm@gmail.com
                donnam@bcm.edu
                rodrigo.nunes.da.fonseca@gmail.com
                15054968@brookes.ac.uk
                jiaxinqu@gmail.com
                matthew.ronshaugen@manchester.ac.uk
                c.schomburg@stud.uni-goettingen.de
                aschonauer@brookes.ac.uk
                a.stollewerk@qmul.ac.uk
                montserrat.torres-oliva@biologie.uni-goettingen.de
                natascha.turetzek@biologie.uni-goettingen.de
                bram.vanthournout@ugent.be
                werr@mail.rochester.edu
                carsten.wolff.1@rz.hu-berlin.de
                kworley@bcm.edu
                gbucher1@gwdg.de
                agibbs@bcm.edu
                coddington@si.edu
                hoda@brh.co.jp
                mario.stanke@uni-greifswald.de
                ayoubn@wlu.edu
                nprpic@uni-goettingen.de
                jflot@ulb.ac.be
                nico.posnien@biologie.uni-goettingen.de
                stephenr@bcm.edu
                amcgregor@brookes.ac.uk
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                31 July 2017
                31 July 2017
                2017
                : 15
                Affiliations
                [1 ]ISNI 0000 0001 0726 8331, GRID grid.7628.b, Department of Biological and Medical Sciences, , Oxford Brookes University, ; Gipsy Lane, Oxford, OX3 0BP UK
                [2 ]ISNI 0000 0000 9620 1122, GRID grid.225262.3, Department of Biological Sciences, , University of Massachusetts Lowell, ; 198 Riverside Street, Lowell, MA 01854 USA
                [3 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, Department of Zoology, , University of Wisconsin-Madison, ; 430 Lincoln Drive, Madison, WI 53706 USA
                [4 ]GRID grid.268042.a, Department of Biology, , Washington and Lee University, ; 204 West Washington Street, Lexington, VA 24450 USA
                [5 ]ISNI 0000 0001 2222 1582, GRID grid.266097.c, Department of Biology, , University of California, ; Riverside, Riverside, CA 92521 USA
                [6 ]GRID grid.469946.0, , J. Craig Venter Institute, ; 9714 Medical Center Drive, Rockville, MD 20850 USA
                [7 ]GRID grid.5603.0, , Ernst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, ; Walther-Rathenau-Str. 47, 17487 Greifswald, Germany
                [8 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Department for Developmental Biology, , University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, ; Justus-von-Liebig-Weg 11, 37077 Goettingen, Germany
                [9 ]ISNI 0000 0000 8580 3777, GRID grid.6190.e, Department of Developmental Biology, , University of Cologne, Cologne Biocenter, Institute of Zoology, ; Zuelpicher Straße 47b, 50674 Cologne, Germany
                [10 ]ISNI 0000 0004 0493 3502, GRID grid.417743.2, , JT Biohistory Research Hall, ; 1-1 Murasaki-cho, Takatsuki, Osaka 569-1125 Japan
                [11 ]ISNI 0000 0001 2109 9431, GRID grid.444883.7, , Osaka Medical College, ; Takatsuki, Osaka Japan
                [12 ]ISNI 0000 0004 0461 6769, GRID grid.242287.9, , Institute for Biodiversity Science and Sustainability, California Academy of Sciences, ; 55 Music Concourse Drive, San Francisco, CA 94118 USA
                [13 ]ISNI 0000 0001 1956 2722, GRID grid.7048.b, Department of Bioscience, , Aarhus University, ; Ny Munkegade 116, building 1540, 8000 Aarhus C, Denmark
                [14 ]ISNI 0000 0001 2160 926X, GRID grid.39382.33, Human Genome Sequencing Center, Department of Molecular and Human Genetics, , Baylor College of Medicine, ; One Baylor Plaza, Houston, TX 77030 USA
                [15 ]ISNI 0000 0001 1939 2794, GRID grid.9613.d, Department of Genetics, , Friedrich-Schiller-University Jena, ; Philosophenweg 12, 07743 Jena, Germany
                [16 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Organismic and Evolutionary Biology, , Harvard University, ; 16 Divinity Avenue, Cambridge, MA 02138 USA
                [17 ]Smithsonian National Museum of Natural History, MRC-163, P.O. Box 37012, Washington, DC, 20013-7012 USA
                [18 ]ISNI 0000000121662407, GRID grid.5379.8, Faculty of Biology Medicine and Health, , University of Manchester, ; D.1416 Michael Smith Building, Oxford Road, Manchester, M13 9PT UK
                [19 ]ISNI 0000 0001 2152 1081, GRID grid.241963.b, Division of Invertebrate Zoology, , American Museum of Natural History, ; New York, NY 10024 USA
                [20 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Department of Earth Sciences, , Palaeobiology, Uppsala University, ; Villavägen 16, 75236 Uppsala, Sweden
                [21 ]ISNI 0000 0004 1806 4977, GRID grid.428448.6, , Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide, ; Sevilla, Spain
                [22 ]ISNI 0000 0001 2294 473X, GRID grid.8536.8, , Nucleo em Ecologia e Desenvolvimento SocioAmbiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro (UFRJ), ; Rio de Janeiro, 27941-222 Brazil
                [23 ]ISNI 0000 0001 2171 1133, GRID grid.4868.2, School of Biological and Chemical Sciences, , Queen Mary University of London, ; Mile End Road, E1 4NS London, UK
                [24 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, , Evolution and Optics of Nanostructure group (EON), Biology Department, Ghent University, ; Gent, Belgium
                [25 ]ISNI 0000 0004 1936 9174, GRID grid.16416.34, Biology Department, , University of Rochester, ; Rochester, NY 14627 USA
                [26 ]ISNI 0000 0001 2248 7639, GRID grid.7468.d, , Humboldt-Universität of Berlin, Institut für Biologie, ; Philippstr.13, 10115 Berlin, Germany
                [27 ]ISNI 0000 0001 2364 4210, GRID grid.7450.6, Department of Evolutionary Developmental Genetics, , Johann-Friedrich-Blumenbach-Institute, GZMB, Georg-August-University, ; Göttingen Campus, Justus von Liebig Weg 11, 37077 Göttingen, Germany
                [28 ]ISNI 0000 0004 0373 3971, GRID grid.136593.b, Department of Biological Sciences, , Graduate School of Science, Osaka University, ; Osaka, Japan
                [29 ]ISNI 0000 0001 2348 0746, GRID grid.4989.c, , Université libre de Bruxelles (ULB), Evolutionary Biology & Ecology, ; C.P. 160/12, Avenue F.D. Roosevelt 50, 1050 Brussels, Belgium
                Article
                399
                10.1186/s12915-017-0399-x
                5535294
                28756775
                © McGregor et al. 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: NHGRI U54 HG003273
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS-0951886
                Funded by: Leverhulme Trust (GB)
                Award ID: VF-2012-016
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Funded by: Deutsche Forschungsgemeinschaft
                Award ID: PR 1109/4-1, PR 1109/7-1 and PR 1109/6-1
                Award ID: PO 1648/3-1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001663, Volkswagen Foundation;
                Award ID: 85 983
                Award Recipient :
                Funded by: L'Oréal Deutschland and the Deutsche UNESCO-Kommission
                Funded by: Swedish Research Council
                Award ID: 621-2011-4703
                Award Recipient :
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                © The Author(s) 2017

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