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Nature. 2016 Oct 20;538(7625):336-343. doi: 10.1038/nature19840.

Genome evolution in the allotetraploid frog Xenopus laevis.

Author information

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.
2
US Department of Energy Joint Genome Institute, Walnut Creek, California 94598, USA.
3
Department of Applied Molecular Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 464-8601, Japan.
4
Department of Molecular Biosciences, Center for Systems and Synthetic Biology, University of Texas at Austin, Austin, Texas 78712, USA.
5
Department of Biomedical Engineering, School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan 689-798, Republic of Korea.
6
Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.
7
Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8526, Japan.
8
Laboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University, N10W8, Kita-ku, Sapporo 060-0810, Japan.
9
Division of Human Sciences, Graduate School of Integrated Arts and Sciences, Hiroshima University, 1-7-1 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8521, Japan.
10
Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki, Miura, Kanagawa 238-0225, Japan.
11
Radboud University, Faculty of Science, Department of Molecular Developmental Biology, 259 RIMLS, M850/2.97, Geert Grooteplein 28, Nijmegen 6525 GA, the Netherlands.
12
Salk Institute, Molecular Neurobiology Laboratory, La Jolla, San Diego, California 92037, USA.
13
Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, San Diego, California 92037, USA.
14
Department of Animal Bioscience, Nagahama Institute of Bio-Science and Technology, 1266 Tamura, Nagahama, Shiga 526-0829, Japan.
15
Institute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine, 2-2-2 Iida-Nishi, Yamagata, Yamagata 990-9585, Japan.
16
Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan.
17
Dovetail Genomics LLC. Santa Cruz, California 95060, USA.
18
Department of Genome Medicine, National Research Institute for Child Health and Development, NCCHD, 2-10-1, Okura, Setagaya-ku, Tokyo 157-8535, Japan.
19
Department of Life Science and Technology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan.
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.
21
Institute of Institution of Liberal Arts and Fundamental Education, Tokushima University, 1-1 Minamijosanjima-cho, Tokushima 770-8502, Japan.
22
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.
23
Department of Life Science, Faculty of Science, Rikkyo University, 3-34-1 Nishi-Ikebukuro, Toshima-ku, Tokyo 171-8501, Japan.
24
Department of Microbiology and Immunology, University of Maryland, 655 W Baltimore St, Baltimore, Maryland 21201, USA.
25
Kitasato Institute for Life Sciences, Kitasato University, 5-9-1 Shirokane Minato-ku, Tokyo 108-8641, Japan.
26
HudsonAlpha Institute of Biotechnology, Huntsville, Alabama 35806, USA.
27
Department of Human Genetics, University of Chicago, 920 E. 58th St, CLSC 431F, Chicago, Illinois 60637, USA.
28
Department of Computational Biology and Medical Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa-shi, Chiba 277-8568, Japan.
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.
30
Division of Morphogenesis, Department of Developmental Biology, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
31
University of California, Berkeley, Department of Molecular and Cell Biology, Life Sciences Addition #3200, Berkeley California 94720-3200, USA.
32
Illumina Inc., 25861 Industrial Blvd, Hayward, California 94545, USA.
33
Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle Washington 98195-5065, USA.
34
Department of Biology, University of Virginia, Charlottesville, Virginia 22904, USA.
35
Department of Biology, Faculty of Science, Niigata University, 8050, Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan.
36
Department of Microbiology &Immunology, University of Rochester Medical Center, Rochester, New York 14642, USA.
37
Division of Developmental Biology, Cincinnati Children's Research Foundation, Cincinnati, Ohio 45229-3039, USA.
38
Department of Biological Sciences, University of Calgary, Alberta T2N 1N4, Canada.
39
Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan.
40
The University of Iowa, Department of Biology, 257 Biology Building, Iowa City, Iowa 52242-1324, USA.
41
Department of Zoology and Evolutionary Biology, University of Basel, Basel CH-4051, Switzerland.
42
Department of Biological Sciences, School of Science, Kitasato University, 1-15-1 Minamiku, Sagamihara, Kanagawa 252-0373, Japan.
43
Department of Basic Biology, SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
44
Principles of Informatics, National Institute of Informatics, 2-1-2 Hitotsubashi, Chiyoda-ku, Tokyo 101-8430, Japan.
45
Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), 1111 Yata, Mishima, Shizoka 411-8540, Japan.
46
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.

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.

PMID:
27762356
PMCID:
PMC5313049
DOI:
10.1038/nature19840
[Indexed for MEDLINE]
Free PMC Article

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