Genome evolution in the allotetraploid frog Xenopus laevis
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, m...
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| Published in | Nature (London) Vol. 538; no. 7625; pp. 336 - 343 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
20.10.2016
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| 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.
The two homoeologous subgenomes in the allotetraploid frog
Xenopus laevis
evolved asymmetrically; one often retained the ancestral state, whereas the other experienced gene loss, deletion, rearrangement and reduced gene expression.
Genomic evolution in
Xenopus laevis
Xenopus laevis
, also known as the African clawed frog or platanna, is an important model organism that is used in the study of vertebrate cell and developmental biology. It is a palaeotetraploid—the product of genome duplications that occurred many millions of years ago. This makes
X. laevis
ideal for the study of polyploidy, but has greatly complicated genome sequencing. Here an international research collaboration reports the
X. laevis
genome sequence and compares it to that of the related
X. tropicalis
. Their analyses confirm that
X. laevis
is an allotetraploid and distinguishes two subgenomes that evolved asymmetrically—one often retained the ancestral state and the other was subject to gene loss, deletion, rearrangement and reduced expression. The two diploid progenitor species diverged about 34 million years ago, combining to form an allotetraploid about 18 million years ago. |
|---|---|
| AbstractList | 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.
The two homoeologous subgenomes in the allotetraploid frog
Xenopus laevis
evolved asymmetrically; one often retained the ancestral state, whereas the other experienced gene loss, deletion, rearrangement and reduced gene expression.
Genomic evolution in
Xenopus laevis
Xenopus laevis
, also known as the African clawed frog or platanna, is an important model organism that is used in the study of vertebrate cell and developmental biology. It is a palaeotetraploid—the product of genome duplications that occurred many millions of years ago. This makes
X. laevis
ideal for the study of polyploidy, but has greatly complicated genome sequencing. Here an international research collaboration reports the
X. laevis
genome sequence and compares it to that of the related
X. tropicalis
. Their analyses confirm that
X. laevis
is an allotetraploid and distinguishes two subgenomes that evolved asymmetrically—one often retained the ancestral state and the other was subject to gene loss, deletion, rearrangement and reduced expression. The two diploid progenitor species diverged about 34 million years ago, combining to form an allotetraploid about 18 million years ago. 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. 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 1718 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. 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 demonstrate the allotetraploid origin of X. laevis by partitioning its genome into two homeologous subgenomes, marked by distinct families of “fossil” transposable elements. Based on the activity of these elements and the age of hundreds of unitary pseudogenes, we estimate that the two diploid progenitor species diverged ~34 million years ago (Mya) and combined to form an allotetraploid ~17–18 Mya. 56% of all genes are retained in two homeologous copies. Protein function, gene expression, and the amount of flanking conserved 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. 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.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. |
| Audience | Academic |
| Author | DuPasquier, Louis Suzuki, Atsushi Yasuoka, Yuuri Shendure, Jay Ohta, Yuko Fukui, Akimasa Yamamoto, Takamasa S. Mawaribuchi, Shuuji Haudenschild, Christian Mitros, Therese Lotay, Vaneet Harland, Richard M. Kondo, Mariko Wallingford, John B. Session, Adam M. Tanaka, Toshiaki Lister, Ryan Burns, Kevin Bogdanovic, Ozren Robert, Jacques Toyoda, Atsushi Ito, Michihiko van Heeringen, Simon J. Schmutz, Jeremy Putnam, Nicholas Kitzman, Jacob Quigley, Ian Grimwood, Jane Carlson, Joseph Suzuki, Yutaka Houston, Douglas W. Paranjpe, Sarita S. Kuroki, Yoko Shu, Shengquiang Kwon, Taejoon Heald, Rebecca Marcotte, Edward M. Hikosaka, Akira Stites, Jonathan van Kruijsbergen, Ila Miller, Kelly Izutsu, Yumi Ogino, Hajime Uno, Yoshinobu Dichmann, Darwin S. Heinz, Sven Watanabe, Minoru Hellsten, Uffe Georgiou, Georgios Takahashi, Shuji Flajnik, Martin F. Michiue, Tatsuo Karimi, Kamran Ito, Yuzuru Lyons, Jessica B. Kinoshita, Tsutomu Jenkins, Jerry Nakayama, Takuya Zorn, Aaron M. Fortriede, Joshua Matsuda, Yoichi Fujiyama, Asao Rokhsar, Daniel S. Vize, Peter D. Chapman, |
| AuthorAffiliation | 4 Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, TX 78712, USA 14 Department of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan 11 Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, 6525 GA Nijmegen, The Netherlands 31 University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA 13 Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA 10 Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan 29 Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Central 5, 1-1-1 Higashi, Tsukuba, Iba |
| AuthorAffiliation_xml | – name: 21 Institute of Institution of Liberal Arts and Fundamental Education, Tokushima University, 1-1 Minamijosanjima-cho, Tokushima, 770-8502, Japan – name: 28 Department of Computational Biology and Medical Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8568, Japan – name: 39 Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan – name: 12 Salk Institute, Molecular Neurobiology Laboratory, La Jolla, CA 92037, USA – name: 43 Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji, Okazaki 444-8585, Aichi, Japan – name: 15 Institute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine, 2-2-2 Iida-Nishi, Yamagata, Yamagata 990-9585, Japan – name: 29 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 – name: 17 Dovetail Genomics LLC. Santa Cruz, CA 95060, USA – name: 1 University of California, Berkeley, Department of Molecular and Cell Biology and Center for Integrative Genomics, Life Sciences Addition #3200, Berkeley California 94720-3200, USA – name: 18 Department of Genome Medicine, National Research Institute for Child Health and Development, NCCHD, 2-10-1, Okura, Setagaya-ku, Tokyo 157-8535, Japan – name: 45 Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), 1111 Yata, Mishima, Shizoka 411-8540, Japan – name: 25 Kitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane Minato-ku Tokyo 108-8641 Japan – name: 44 Principles of Informatics, National Institute of Informatics, 2-1-2 Hitotsubashi, Chiyoda-ku, Tokyo 101-8430, Japan – name: 2 US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA – name: 3 Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan – name: 10 Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan – name: 32 Illumina Inc. present address:Personalis Inc., 1330 O’Brien Drive Menlo Park, CA 94025 – name: 34 Department of Biology, University of Virginia, Charlottesville, VA 22904, USA – name: 4 Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, TX 78712, USA – name: 9 Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan – name: 11 Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, 6525 GA Nijmegen, The Netherlands – name: 20 Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1, Komaba, Meguro-ku, Tokyo 153-8902, Japan – name: 23 Department of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan – name: 14 Department of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan – name: 41 Department of Zoology and Evolutionary Biology, University of Basel, Basel, Switzerland – name: 30 Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan – name: 6 Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan – name: 8 Laboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan – name: 16 Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan – name: 35 Department of Biology, Faculty of Science, Niigata University, 8050, Ikarashi 2-no-cho, Nishi-ku, Niigata, 950-2181, Japan – name: 31 University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA – name: 46 Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan – name: 38 Department of Biological Sciences, University of Calgary, Alberta T2N1N4, Canada – name: 27 Department of Human Genetics, University of Chicago, 920 E. 58th St, CLSC 431F, Chicago IL 60637, USA – name: 40 The University of Iowa, Department of Biology, 257 Biology Building, Iowa City, IA 52242-1324 – name: 22 Harry Perkins Institute of Medical Research and ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, WA 6009, Australia – name: 33 Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle WA 98195-5065, USA – name: 42 Department of Biological Sciences, School of Science, Kitasato University, 1-15-1 Minamiku, Sagamihara, Kanagawa 252-0373, Japan – name: 7 Institute for Amphibian Biology, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan – name: 37 Division of Developmental Biology, Cincinnati Children’s Research Foundation, Cincinnati, OH, USA – name: 13 Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA – name: 24 Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, MD 21201, USA – name: 5 Department of Biomedical Engineering, School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan, Republic of Korea – name: 26 HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA – name: 19 Department of Biological Sciences, Graduate School of Biocience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan – name: 36 Department of Microbiology & Immunology, University of Rochester Medical Center Rochester, NY 14642, USA |
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Yoichi organization: Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku – sequence: 70 givenname: Gert Jan C. surname: Veenstra fullname: Veenstra, Gert Jan C. organization: Department of Molecular Developmental Biology, Radboud University, Faculty of Science, 259 RIMLS, M850/2.97 – sequence: 71 givenname: Asao surname: Fujiyama fullname: Fujiyama, Asao organization: Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, Principles of Informatics, National Institute of Informatics, 2-1-2 Hitotsubashi, Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies) – sequence: 72 givenname: Richard M. surname: Harland fullname: Harland, Richard M. email: harland@berkeley.edu organization: Department of Molecular and Cell Biology and Center for Integrative Genomics, University of California, Berkeley, Life Sciences Addition #3200 – sequence: 73 givenname: Masanori surname: Taira fullname: Taira, Masanori email: m_taira@bs.s.u-tokyo.ac.jp organization: Department of Biological Sciences, Graduate School of Science, The University of Tokyo – sequence: 74 givenname: Daniel S. surname: Rokhsar fullname: Rokhsar, Daniel S. email: dsrokhsar@gmail.com organization: Department of Molecular and Cell Biology and Center for Integrative Genomics, University of California, Berkeley, Life Sciences Addition #3200, US Department of Energy Joint Genome Institute, Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27762356$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1615264$$D View this record in Osti.gov |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 ObjectType-Article-2 ObjectType-Feature-1 content type line 23 Eunice Kennedy Shriver National Institute for Child Health & Human Development (NICHD) National Human Genome Research Institute (NHGRI) National Heart, Lung and Blood Institute (NHLBI) National Institutes of Health (NIH) Cancer Prevention and Research Institute of Texas (CPRIT) AC02-05CH11231; HD065705; HD080708; P41 HD064556; GM086321; 221S0002; 24590232; 25440180; 15K14521; 15K07082; 22570137; 25460245; 23370059; 23113004; 25251026; 22127007; 1.150094.01; 1.150043.01; 1.160060.01; F1515; R01HD069344; 863.12.002; DE140101962; 1S10OD018174 USDOE Office of Science (SC), Biological and Environmental Research (BER) National Science Foundation (NSF) Okinawa Institute for Science and Technology Graduate University UNIST Research Fund SURF Foundation Japan Society for the Promotion of Science (JSPS) Australian Research Council (ARC) National Institute of Allergy and Infectious Diseases (NIAID) Netherlands Organization for Scientific Research (NWO) Hiroshima University Phoenix Leader Education Program Welch Foundation Ministry of Education, Culture, Sports, Science and Technology (MEXT) National Institute of General Medical Sciences (NIGMS) equal contribution |
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| Snippet | 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... 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... |
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| SubjectTerms | 38/91 45/23 45/71 49/15 49/39 631/181/735 631/208/212/2304 64/114 Amphibians Animals Artificial chromosomes BASIC BIOLOGICAL SCIENCES Chromosomes - genetics Conserved Sequence - genetics Deoxyribonucleic acid Diploidy DNA DNA methylation DNA Transposable Elements - genetics Epigenetics Evolution, Molecular Female Frogs Gene Deletion Gene expression Gene Expression Profiling Genome - genetics Genome evolution Genomes Humanities and Social Sciences Karyotype Molecular evolution Molecular Sequence Annotation multidisciplinary Mutagenesis - genetics Phylogeny Physiological aspects Polyploidy Proteins Pseudogenes Science Tetraploidy Xenopus - genetics Xenopus laevis - genetics |
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| Title | Genome evolution in the allotetraploid frog Xenopus laevis |
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