ArticleNature2016
Genome evolution in the allotetraploid frog Xenopus laevis.
Open access · hybridAbstract readComparative Study
In one paragraph
Article in Nature, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 542 papers.
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542citing papers in PubMed
59.5field-weighted citation impact, top 1% of its field
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Who cites it
542 citing papers in PubMed, 1,029 citations in OpenAlex.
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482 more citing papers are in PubMed but not listed here.
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Authors and funding
74 authors at 20 institutions in 6 countries.
Adam M SessionUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Yoshinobu UnoDepartment of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.
Taejoon KwonDepartment of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
Jarrod A ChapmanUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Atsushi ToyodaCenter for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.
Shuji TakahashiAmphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan.
Akimasa FukuiLaboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan.
Akira HikosakaDivision of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan.
Atsushi SuzukiAmphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan.
Mariko KondoMisaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan.
Simon J van HeeringenRadboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Ian QuigleySalk Institute, Molecular Neurobiology Laboratory, La Jolla, San Diego, California 92037, USA.
Sven HeinzSalk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA.
Hajime OginoDepartment of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan.
Haruki OchiInstitute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine, 2-2-2 Iida-Nishi, Yamagata, Yamagata 990-9585, Japan.
Uffe HellstenUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Jessica B LyonsUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Oleg SimakovMolecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
Nicholas PutnamDovetail Genomics LLC. Santa Cruz, California 95060, USA.
Jonathan StitesDovetail Genomics LLC. Santa Cruz, California 95060, USA.
Yoko KurokiDepartment of Genome Medicine, National Research Institute for Child Health and Development, NCCHD, 2-10-1, Okura, Setagaya-ku, Tokyo 157-8535, Japan.
Toshiaki TanakaDepartment of Life Science and Technology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan.
Tatsuo MichiueDepartment of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1, Komaba, Meguro-ku, Tokyo 153-8902, Japan.
Minoru WatanabeInstitute of Institution of Liberal Arts and Fundamental Education, Tokushima University, 1-1 Minamijosanjima-cho, Tokushima 770-8502, Japan.
Ozren BogdanovicHarry Perkins Institute of Medical Research and ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia 6009, Australia.
Ryan ListerHarry Perkins Institute of Medical Research and ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Western Australia 6009, Australia.
Georgios GeorgiouRadboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Sarita S ParanjpeRadboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Ila van KruijsbergenRadboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Shengquiang ShuUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Joseph CarlsonUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Tsutomu KinoshitaDepartment of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan.
Yuko OhtaDepartment of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA.
Shuuji MawaribuchiKitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane Minato-ku, Tokyo 108-8641, Japan.
Jerry JenkinsUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Jane GrimwoodUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Jeremy SchmutzUS Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Therese MitrosUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Sahar V MozaffariDepartment of Human Genetics, University of Chicago, 920 E. 58th St, CLSC 431F, Chicago, Illinois 60637, USA.
Yutaka SuzukiDepartment of Computational Biology and Medical Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8568, Japan.
Yoshikazu HaramotoBiotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Central 5, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, Japan.
Takamasa S YamamotoDivision of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Chiyo TakagiDivision of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Rebecca HealdUniversity of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA.
Kelly MillerUniversity of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA.
Christian HaudenschildIllumina Inc., 25861 Industrial Blvd, Hayward, California 94545, USA.
Jacob KitzmanDepartment of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA.
Takuya NakayamaDepartment of Biology, University of Virginia, Charlottesville, Virginia 22904, USA.
Yumi IzutsuDepartment of Biology, Faculty of Science, Niigata University, 8050, Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan.
Jacques RobertDepartment of Microbiology &Immunology, University of Rochester Medical Center, Rochester, New York 14642, USA.
Joshua FortriedeDivision of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Kevin BurnsDivision of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Vaneet LotayDepartment of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Kamran KarimiDepartment of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Yuuri YasuokaMarine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan.
Darwin S DichmannUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Martin F FlajnikDepartment of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA.
Douglas W HoustonThe University of Iowa, Department of Biology, 257 Biology Building, Iowa City, Iowa 52242-1324, USA.
Jay ShendureDepartment of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA.
Louis DuPasquierDepartment of Zoology and Evolutionary Biology, University of Basel, Basel CH-4051, Switzerland.
Peter D VizeDepartment of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Aaron M ZornDivision of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Michihiko ItoDepartment of Biological Sciences, School of Science, Kitasato University, 1-15-1 Minamiku, Sagamihara, Kanagawa 252-0373, Japan.
Edward M MarcotteDepartment of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
John B WallingfordDepartment of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
Yuzuru ItoBiotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Central 5, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, Japan.
Makoto AsashimaBiotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Central 5, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8565, Japan.
Naoto UenoDivision of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Yoichi MatsudaDepartment of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.
Gert Jan C VeenstraRadboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Asao FujiyamaCenter for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.
Richard M HarlandUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Masanori TairaDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
Daniel S RokhsarUniversity of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Joint Genome Institute · USUniversity of California, Berkeley · USThe University of Tokyo · JPCincinnati Children's Hospital Medical Center · USHiroshima University · JPNational Institute for Basic Biology · JPNational Institute of Advanced Industrial Science and Technology · JPOkinawa Institute of Science and Technology Graduate University · JPRadboud University Medical Center · NLThe University of Texas at Austin · USUniversity of Calgary · CADovetail Genomics (United States) · USNagoya University · JPRadboud Institute for Molecular Life Sciences · NLSalk Institute for Biological Studies · USUniversity of Maryland, Baltimore · USUniversity of Washington · USUniversity of Western Australia · AUHokkaido University · JPIllumina (United States) · US
Funding
Xenbase: the Xenopus Model Organism KnowledgebaseP41HD064556 · NICHD · CINCINNATI CHILDRENS HOSP MED CTR · PI PETER D VIZE, Aaron M Zorn · 2010 to 2026
$24.9MGENOMICST32HG000047 · NHGRI · UNIVERSITY OF CALIFORNIA BERKELEY · PI RASMUS NIELSEN, Daniel Soleyman Rokhsar · 2000 to 2026
$13.5MMechanisms of mitosis and size control in XenopusR35GM118183 · NIGMS · UNIVERSITY OF CALIFORNIA BERKELEY · PI HEALD, REBECCA W · 2016 to 2025
$8.2MGene Expression in Amphibian DevlopementR01GM042341 · NIGMS · UNIVERSITY OF CALIFORNIA BERKELEY · PI HARLAND, RICHARD M · 1988 to 2016
$5.7MDevelopment and function in mucociliary epitheliaR01HL117164 · NHLBI · UNIVERSITY OF TEXAS AT AUSTIN · PI John B Wallingford · 2013 to 2026
$4.7MComparative Genetics and Genomics of XenopusR01GM086321 · NIGMS · UNIVERSITY OF CALIFORNIA BERKELEY · PI HARLAND, RICHARD M, ROKHSAR, DANIEL SOLEYMAN · 2009 to 2016
$2.5MSystematic improvement of Xenopus gene annotations and reference genomesR01HD080708 · NICHD · UNIVERSITY OF CALIFORNIA BERKELEY · PI ROKHSAR, DANIEL SOLEYMAN · 2014 to 2017
$2.2MEvolution of Adaptive ImmunityR01OD010549 · OD · UNIVERSITY OF MARYLAND BALTIMORE · PI FLAJNIK, MARTIN F · 2013 to 2017
$1.7MEpigenome maps of regulatory activity in Xenopus tropicalis embryosR01HD069344 · NICHD · STICHTING RADBOUD UNIVERSITEIT · PI VEENSTRA, GERT JAN C. · 2011 to 2015
$1.4MControl of collective cell movement by planar cell polarity signalingR01GM104853 · NIGMS · UNIVERSITY OF TEXAS AT AUSTIN · PI WALLINGFORD, JOHN B · 2015 to 2018
$1.3MDevelopmental control of cell polarity in vertebrate embryos.R01GM086627 · NIGMS · UNIVERSITY OF TEXAS AT AUSTIN · PI WALLINGFORD, JOHN B · 2009 to 2010
$529kIllumina Sequencer to Facilitate Functional Genomics at BerkeleyS10RR027303 · NCRR · UNIVERSITY OF CALIFORNIA BERKELEY · PI TAYLOR, JOHN W. · 2010 to 2010
$500kNHGRI NIH HHS T32 HG000047NHLBI NIH HHS R01 HL117164NICHD NIH HHS P41 HD064556NICHD NIH HHS R01 HD069344NICHD NIH HHS R01 HD080708NICHD NIH HHS R21 HD084072NIGMS NIH HHS R01 GM042341NIGMS NIH HHS R01 GM086321NIGMS NIH HHS R01 GM086627NIGMS NIH HHS R01 GM104853NIGMS NIH HHS R21 GM119021NIGMS NIH HHS R35 GM118183NIH HHS R01 OD010549United States GM086321United States HD065705United States HD080708
Abstract
To explore the origins and consequences of tetraploidy in the African clawed frog, we sequenced the Xenopus laevis genome and compared it to the related diploid X. tropicalis genome. We characterize the allotetraploid origin of X. laevis by partitioning its genome into two homoeologous subgenomes, marked by distinct families of 'fossil' transposable elements. On the basis of the activity of these elements and the age of hundreds of unitary pseudogenes, we estimate that the two diploid progenitor species diverged around 34 million years ago (Ma) and combined to form an allotetraploid around 17-18 Ma. More than 56% of all genes were retained in two homoeologous copies. Protein function, gene expression, and the amount of conserved flanking sequence all correlate with retention rates. The subgenomes have evolved asymmetrically, with one chromosome set more often preserving the ancestral state and the other experiencing more gene loss, deletion, rearrangement, and reduced gene expression.
Indexed as
Evolution, MolecularPhylogenyTetraploidyAnimalsChromosomesConserved SequenceDiploidyDNA Transposable ElementsFemaleGene DeletionGene Expression ProfilingGenomeKaryotypeMolecular Sequence AnnotationMutagenesisPseudogenesDNA Transposable Elements
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