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PMID: 27762356 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Genome evolution in the allotetraploid frog Xenopus laevis.

Nature ·Vol. 538 ·No. 7625 ·2016-00-20 ·Pages 336-343

Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S, Fukui A, Hikosaka A, Suzuki A, Kondo M, van Heeringen SJ, Quigley I, Heinz S, Ogino H, Ochi H, Hellsten U, Lyons JB, Simakov O, Putnam N, Stites J, Kuroki Y, Tanaka T, Michiue T, Watanabe M, Bogdanovic O, Lister R, Georgiou G, Paranjpe SS, van Kruijsbergen I, Shu S, Carlson J, Kinoshita T, Ohta Y, Mawaribuchi S, Jenkins J, Grimwood J, Schmutz J, Mitros T, Mozaffari SV, Suzuki Y, Haramoto Y, Yamamoto TS, Takagi C, Heald R, Miller K, Haudenschild C, Kitzman J, Nakayama T, Izutsu Y, Robert J, Fortriede J, Burns K, Lotay V, Karimi K, Yasuoka Y, Dichmann DS, Flajnik MF, Houston DW, Shendure J, DuPasquier L, Vize PD, Zorn AM, Ito M, Marcotte EM, Wallingford JB, Ito Y, Asashima M, Ueno N, Matsuda Y, Veenstra GJ, Fujiyama A, Harland RM, Taira M, Rokhsar DS

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.

MeSH Terms
Animals Chromosomes/genetics Conserved Sequence/genetics DNA Transposable Elements/genetics Diploidy Evolution, Molecular Female Gene Deletion Gene Expression Profiling Genome/genetics Karyotype Molecular Sequence Annotation Mutagenesis/genetics Phylogeny Pseudogenes Tetraploidy Xenopus/genetics Xenopus laevis/genetics
Chemicals
DNA Transposable Elements
Authors & Affiliations
74 authors, click to expand affiliations / ORCID
Session Adam M
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA. | US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Uno Yoshinobu
Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.
Kwon Taejoon
Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA. | Department of Biomedical Engineering, School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan 689-798, Republic of Korea.
Chapman Jarrod A
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Toyoda Atsushi
Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.
Takahashi Shuji
Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan.
Fukui Akimasa
Laboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan.
Hikosaka Akira
Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan.
Suzuki Atsushi
Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan.
Kondo Mariko
Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan.
van Heeringen Simon J
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Quigley Ian
Salk Institute, Molecular Neurobiology Laboratory, La Jolla, San Diego, California 92037, USA.
Heinz Sven
Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA.
Ogino Hajime
Department of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan.
Ochi Haruki
Institute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine, 2-2-2 Iida-Nishi, Yamagata, Yamagata 990-9585, Japan.
Hellsten Uffe
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Lyons Jessica B
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Simakov Oleg
Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
Putnam Nicholas
Dovetail Genomics LLC. Santa Cruz, California 95060, USA.
Stites Jonathan
Dovetail Genomics LLC. Santa Cruz, California 95060, USA.
Kuroki Yoko
Department of Genome Medicine, National Research Institute for Child Health and Development, NCCHD, 2-10-1, Okura, Setagaya-ku, Tokyo 157-8535, Japan.
Tanaka Toshiaki
Department of Life Science and Technology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan.
Michiue Tatsuo
Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1, Komaba, Meguro-ku, Tokyo 153-8902, Japan.
Watanabe Minoru
Institute of Institution of Liberal Arts and Fundamental Education, Tokushima University, 1-1 Minamijosanjima-cho, Tokushima 770-8502, Japan.
Bogdanovic Ozren
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.
Lister Ryan
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.
Georgiou Georgios
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Paranjpe Sarita S
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
van Kruijsbergen Ila
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Shu Shengquiang
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Carlson Joseph
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
Kinoshita Tsutomu
Department of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan.
Ohta Yuko
Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA.
Mawaribuchi Shuuji
Kitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane Minato-ku, Tokyo 108-8641, Japan.
Jenkins Jerry
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA. | HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA.
Grimwood Jane
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA. | HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA.
Schmutz Jeremy
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA. | HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA.
Mitros Therese
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Mozaffari Sahar V
Department of Human Genetics, University of Chicago, 920 E. 58th St, CLSC 431F, Chicago, Illinois 60637, USA.
Suzuki Yutaka
Department of Computational Biology and Medical Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8568, Japan.
Haramoto Yoshikazu
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.
Yamamoto Takamasa S
Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Takagi Chiyo
Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Heald Rebecca
University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA.
Miller Kelly
University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA.
Haudenschild Christian
Illumina Inc., 25861 Industrial Blvd, Hayward, California 94545, USA.
Kitzman Jacob
Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA.
Nakayama Takuya
Department of Biology, University of Virginia, Charlottesville, Virginia 22904, USA.
Izutsu Yumi
Department of Biology, Faculty of Science, Niigata University, 8050, Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan.
Robert Jacques
Department of Microbiology &Immunology, University of Rochester Medical Center, Rochester, New York 14642, USA.
Fortriede Joshua
Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Burns Kevin
Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Lotay Vaneet
Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Karimi Kamran
Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Yasuoka Yuuri
Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan.
Dichmann Darwin S
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Flajnik Martin F
Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA.
Houston Douglas W
The University of Iowa, Department of Biology, 257 Biology Building, Iowa City, Iowa 52242-1324, USA.
Shendure Jay
Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA.
DuPasquier Louis
Department of Zoology and Evolutionary Biology, University of Basel, Basel CH-4051, Switzerland.
Vize Peter D
Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
Zorn Aaron M
Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
Ito Michihiko
Department of Biological Sciences, School of Science, Kitasato University, 1-15-1 Minamiku, Sagamihara, Kanagawa 252-0373, Japan.
Marcotte Edward M
Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
Wallingford John B
Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
Ito Yuzuru
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.
Asashima Makoto
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.
Ueno Naoto
Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan. | Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
Matsuda Yoichi
Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.
Veenstra Gert Jan C
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
Fujiyama Asao
Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan. | Principles of Informatics, National Institute of Informatics, 2-1-2 Hitotsubashi, Chiyoda-ku, Tokyo 101-8430, Japan. | Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), 1111 Yata, Mishima, Shizoka 411-8540, Japan.
Harland Richard M
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA.
Taira Masanori
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
Rokhsar Daniel S
University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley, California 94720-3200, USA. | US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA. | Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
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Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
DOI
10.1038/nature19840
Published
2016-00-20
Pages
336-343
Language
English
Region
England
NLM ID
0410462
PMCID
PMC5313049
Subset
IM
Grants
HD065705 · International
GM086321 · International
NHGRI NIH HHS · T32 HG000047 · United States
NIGMS NIH HHS · R35 GM118183 · United States
NICHD NIH HHS · P41 HD064556 · United States
NIGMS NIH HHS · R01 GM042341 · United States
NICHD NIH HHS · R01 HD069344 · United States
NIGMS NIH HHS · R01 GM086627 · United States
NIGMS NIH HHS · R01 GM086321 · United States
NIGMS NIH HHS · R01 GM104853 · United States
NIGMS NIH HHS · R21 GM119021 · United States
NCRR NIH HHS · S10 RR027303 · United States
NIH HHS · R01 OD010549 · United States
NHLBI NIH HHS · R01 HL117164 · United States
NICHD NIH HHS · R21 HD084072 · United States
NICHD NIH HHS · R01 HD080708 · United States
HD080708 · International
Corrections
CommentIn
PMID: 27762363
External Links
PubMed source DOI: 10.1038/nature19840 PMC Full Text View journal details
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