Genome evolution in the allotetraploid frog Xenopus laevis

Adam M Session; Yoshinobu Uno; Taejoon Kwon; Jarrod A Chapman; Atsushi Toyoda; Shuji Takahashi; Akimasa Fukui; Akira Hikosaka; Atsushi Suzuki; Mariko Kondo; Simon J van Heeringen; Ian Quigley; Sven Heinz; Hajime Ogino; Haruki Ochi; Uffe Hellsten; Jessica B Lyons; Oleg Simakov; Nicholas Putnam; Jonathan Stites; Yoko Kuroki; Toshiaki Tanaka; Tatsuo Michiue; Minoru Watanabe; Ozren Bogdanovic; Ryan Lister; Georgios Georgiou; Sarita S Paranjpe; Ila van Kruijsbergen; Shengquiang Shu; Joseph Carlson; Tsutomu Kinoshita; Yuko Ohta; Shuuji Mawaribuchi; Jerry Jenkins; Jane Grimwood; Jeremy Schmutz; Therese Mitros; Sahar V Mozaffari; Yutaka Suzuki; Yoshikazu Haramoto; Chiyo Takagi; Rebecca Heald; Kelly Miller; Christian Haudenschild; Jacob Kitzman; Takuya Nakayama; Yumi Izutsu; Jacques Robert; Joshua Fortriede; Kevin Burns; Vaneet Lotay; Kamran Karimi; Yuuri Yasuoka; Darwin S Dichmann; Martin F Flajnik; Douglas W Houston; Jay Shendure; Louis DuPasquier; Peter D Vize; Aaron M Zorn; Michihiko Ito; Edward M Marcotte; John B Wallingford; Yuzuru Ito; Makoto Asashima; Naoto Ueno; Yoichi Matsuda; Gert Jan C Veenstra; Asao Fujiyama; Richard M Harland; Masanori Taira; Daniel S Rokhsar; Takamasa S Yamamoto

doi:10.1038/nature19840

Back

Genome evolution in the allotetraploid frog Xenopus laevis

Journal article

Open access

Peer reviewed

Genome evolution in the allotetraploid frog Xenopus laevis

Adam M Session, Yoshinobu Uno, Taejoon Kwon, Jarrod A Chapman, Atsushi Toyoda, Shuji Takahashi, Akimasa Fukui, Akira Hikosaka, Atsushi Suzuki, Mariko Kondo, …

Nature (London), Vol.538(7625), pp.336-343

10/20/2016

DOI: 10.1038/nature19840

PMCID: PMC5313049

PMID: 27762356

Files and links (1)

url

https://doi.org/10.1038/nature19840View

Published (Version of record) Open Access

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.

Conserved Sequence - genetics

Xenopus - genetics

Molecular Sequence Annotation

Genome - genetics

Mutagenesis - genetics

Gene Expression Profiling

Phylogeny

Tetraploidy

Diploidy

Animals

Pseudogenes

Chromosomes - genetics

Gene Deletion

DNA Transposable Elements - genetics

Female

Xenopus laevis - genetics

Karyotype

Evolution, Molecular

Details

Title: Subtitle: Genome evolution in the allotetraploid frog Xenopus laevis
Creators: Adam M Session - US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
Yoshinobu Uno - Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan
Taejoon Kwon - Department of Biomedical Engineering, School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan 689-798, Republic of Korea
Jarrod A Chapman - US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
Atsushi Toyoda - Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan
Shuji Takahashi - Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan
Akimasa Fukui - Laboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan
Akira Hikosaka - Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan
Atsushi Suzuki - Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan
Mariko Kondo - Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan
Simon J van Heeringen - Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands
Ian Quigley - Salk Institute, Molecular Neurobiology Laboratory, La Jolla, San Diego, California 92037, USA
Sven Heinz - Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA
Hajime Ogino - Department of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan
Haruki Ochi - Institute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine, 2-2-2 Iida-Nishi, Yamagata, Yamagata 990-9585, Japan
Uffe Hellsten - US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
Jessica B Lyons - University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA
Oleg Simakov - Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan
Nicholas Putnam - Dovetail Genomics LLC. Santa Cruz, California 95060, USA
Jonathan Stites - Dovetail Genomics LLC. Santa Cruz, California 95060, USA
Yoko Kuroki - Department of Genome Medicine, National Research Institute for Child Health and Development, NCCHD, 2-10-1, Okura, Setagaya-ku, Tokyo 157-8535, Japan
Toshiaki Tanaka - Department of Life Science and Technology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan
Tatsuo Michiue - Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1, Komaba, Meguro-ku, Tokyo 153-8902, Japan
Minoru Watanabe - Institute of Institution of Liberal Arts and Fundamental Education, Tokushima University, 1-1 Minamijosanjima-cho, Tokushima 770-8502, Japan
Ozren Bogdanovic - Harry 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 Lister - Harry 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 Georgiou - Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands
Sarita S Paranjpe - Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands
Ila van Kruijsbergen - Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands
Shengquiang Shu - US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
Joseph Carlson - US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA
Tsutomu Kinoshita - Department of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan
Yuko Ohta - Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA
Shuuji Mawaribuchi - Kitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane Minato-ku, Tokyo 108-8641, Japan
Jerry Jenkins - HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA
Jane Grimwood - HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA
Jeremy Schmutz - HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA
Therese Mitros - University 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 Mozaffari - Department of Human Genetics, University of Chicago, 920 E. 58th St, CLSC 431F, Chicago, Illinois 60637, USA
Yutaka Suzuki - Department of Computational Biology and Medical Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8568, Japan
Yoshikazu Haramoto - Biotechnology 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
Chiyo Takagi - Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan
Rebecca Heald - University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA
Kelly Miller - University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA
Christian Haudenschild - Illumina Inc., 25861 Industrial Blvd, Hayward, California 94545, USA
Jacob Kitzman - Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA
Takuya Nakayama - Department of Biology, University of Virginia, Charlottesville, Virginia 22904, USA
Yumi Izutsu - Department of Biology, Faculty of Science, Niigata University, 8050, Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan
Jacques Robert - Department of Microbiology &Immunology, University of Rochester Medical Center, Rochester, New York 14642, USA
Joshua Fortriede - Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA
Kevin Burns - Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA
Vaneet Lotay - Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada
Kamran Karimi - Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada
Yuuri Yasuoka - Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan
Darwin S Dichmann - University 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 Flajnik - Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA
Douglas W Houston - The University of Iowa, Department of Biology, 257 Biology Building, Iowa City, Iowa 52242-1324, USA
Jay Shendure - Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA
Louis DuPasquier - Department of Zoology and Evolutionary Biology, University of Basel, Basel CH-4051, Switzerland
Peter D Vize - Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada
Aaron M Zorn - Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA
Michihiko Ito - Department of Biological Sciences, School of Science, Kitasato University, 1-15-1 Minamiku, Sagamihara, Kanagawa 252-0373, Japan
Edward M Marcotte - Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA
John B Wallingford - Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA
Yuzuru Ito - Biotechnology 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 Asashima - Biotechnology 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 Ueno - Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan
Yoichi Matsuda - Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan
Gert Jan C Veenstra - Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands
Asao Fujiyama - Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), 1111 Yata, Mishima, Shizoka 411-8540, Japan
Richard M Harland - University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA
Masanori Taira - Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
Daniel S Rokhsar - Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan
Takamasa S Yamamoto - National Institute for Basic Biology
Resource Type: Journal article
Publication Details: Nature (London), Vol.538(7625), pp.336-343
DOI: 10.1038/nature19840
PMID: 27762356
PMCID: PMC5313049
NLM abbreviation: Nature
ISSN: 1476-4687
eISSN: 1476-4687
Publisher: England
Grant note: R01 GM086627 / NIGMS NIH HHS R21 HD084072 / NICHD NIH HHS S10 RR027303 / NCRR NIH HHS R01 HL117164 / NHLBI NIH HHS T32 HG000047 / NHGRI NIH HHS R21 GM119021 / NIGMS NIH HHS P41 HD064556 / NICHD NIH HHS R01 GM042341 / NIGMS NIH HHS R35 GM118183 / NIGMS NIH HHS R01 OD010549 / NIH HHS R01 GM086321 / NIGMS NIH HHS R01 HD080708 / NICHD NIH HHS R01 HD069344 / NICHD NIH HHS R01 GM104853 / NIGMS NIH HHS
Language: English
Date published: 10/20/2016
Academic Unit: Biology
Record Identifier: 9983992054502771

Metrics

30 Record Views

725 Times Cited - Web of Science