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      Genome evolution in the allotetraploid frog Xenopus laevis

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      1 , 2 , 3 , 4 , 5 , 2 , 6 , 7 , 8 , 9 , 7 , 10 , 11 , 12 , 13 , 14 , 15 , 2 , 1 , 16 , 17 , 17 , 18 , 19 , 20 , 21 , 22 ,   22 , 11 , 11 , 11 , 2 , 2 , 23 , 24 , 25 , 2 , 26 , 2 , 26 , 2 , 26 , 1 , 27 , 28 , 29 , 30 , 30 , 31 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 37 , 38 , 38 , 39 , 1 , 24 , 40 , 33 , 41 , 38 , 37 , 42 , 4 , 4 , 29 , 29 , 30 , 43 , 3 , 11 , 6 , 44 , 45 , 1 , , 46 , , 1 , 2 , 16 ,
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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 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.

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          The significance of responses of the genome to challenge.

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            Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia.

            The duplication of entire genomes has long been recognized as having great potential for evolutionary novelties, but the mechanisms underlying their resolution through gene loss are poorly understood. Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event. Genes from the same metabolic pathway or protein complex have common patterns of gene loss, and highly expressed genes are over-retained after all duplications. The conclusion of this analysis is that many genes are maintained after whole-genome duplication not because of functional innovation but because of gene dosage constraints.
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              Whole-genome duplication in teleost fishes and its evolutionary consequences.

              Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                27 January 2017
                20 October 2016
                20 April 2017
                : 538
                : 7625
                : 336-343
                Affiliations
                [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, TX 78712, USA
                [5 ]Department of Biomedical Engineering, School of Life Sciences, Ulsan National Institute of Science and Technology, Ulsan, Republic of Korea
                [6 ]Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan
                [7 ]Institute for Amphibian Biology, 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, 6525 GA Nijmegen, The Netherlands
                [12 ]Salk Institute, Molecular Neurobiology Laboratory, La Jolla, CA 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, CA 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 Biological Sciences, Graduate School of Biocience and Biotechnology, 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, WA 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, MD 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 IL 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. present address:Personalis Inc., 1330 O’Brien Drive Menlo Park, CA 94025
                [33 ]Department of Genome Sciences, University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE, Seattle WA 98195-5065, USA
                [34 ]Department of Biology, University of Virginia, Charlottesville, VA 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, NY 14642, USA
                [37 ]Division of Developmental Biology, Cincinnati Children’s Research Foundation, Cincinnati, OH, USA
                [38 ]Department of Biological Sciences, University of Calgary, Alberta T2N1N4, 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, IA 52242-1324
                [41 ]Department of Zoology and Evolutionary Biology, University of Basel, Basel, 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 444-8585, Aichi, 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
                Author notes
                [*]

                equal contribution

                Article
                NIHMS816017
                10.1038/nature19840
                5313049
                27762356
                f495c415-f79f-4486-a84e-73285d669fef

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