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Genome evolution in the allotetraploid frog Xenopus laevis

Author

Listed:
  • Adam M. Session

    (University of California, Berkeley, Life Sciences Addition #3200
    US Department of Energy Joint Genome Institute)

  • Yoshinobu Uno

    (Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku)

  • Taejoon Kwon

    (Center for Systems and Synthetic Biology, University of Texas at Austin
    School of Life Sciences, Ulsan National Institute of Science and Technology)

  • Jarrod A. Chapman

    (US Department of Energy Joint Genome Institute)

  • Atsushi Toyoda

    (Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics)

  • Shuji Takahashi

    (Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama)

  • Akimasa Fukui

    (Laboratory of Tissue and Polymer Sciences, Faculty of Advanced Life Science, Hokkaido University)

  • Akira Hikosaka

    (Graduate School of Integrated Arts and Sciences, Hiroshima University)

  • Atsushi Suzuki

    (Amphibian Research Center, Graduate School of Science, Hiroshima University, 1-3-1 Kagamiyama)

  • Mariko Kondo

    (Misaki Marine Biological Station (MMBS), Graduate School of Science, The University of Tokyo, 1024 Koajiro, Misaki)

  • Simon J. van Heeringen

    (Radboud University, Faculty of Science, 259 RIMLS, M850/2.97)

  • Ian Quigley

    (Salk Institute, Molecular Neurobiology Laboratory, La Jolla)

  • Sven Heinz

    (Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla)

  • Hajime Ogino

    (Nagahama Institute of Bio-Science and Technology)

  • Haruki Ochi

    (Institute for Promotion of Medical Science Research, Yamagata University Faculty of Medicine)

  • Uffe Hellsten

    (US Department of Energy Joint Genome Institute)

  • Jessica B. Lyons

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Oleg Simakov

    (Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University)

  • Nicholas Putnam

    (Dovetail Genomics LLC. Santa Cruz)

  • Jonathan Stites

    (Dovetail Genomics LLC. Santa Cruz)

  • Yoko Kuroki

    (National Research Institute for Child Health and Development, NCCHD)

  • Toshiaki Tanaka

    (Tokyo Institute of Technology)

  • Tatsuo Michiue

    (Graduate School of Arts and Sciences, The University of Tokyo)

  • Minoru Watanabe

    (Institute of Institution of Liberal Arts and Fundamental Education, Tokushima University)

  • Ozren Bogdanovic

    (Harry Perkins Institute of Medical Research and ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia)

  • Ryan Lister

    (Harry Perkins Institute of Medical Research and ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia)

  • Georgios Georgiou

    (Radboud University, Faculty of Science, 259 RIMLS, M850/2.97)

  • Sarita S. Paranjpe

    (Radboud University, Faculty of Science, 259 RIMLS, M850/2.97)

  • Ila van Kruijsbergen

    (Radboud University, Faculty of Science, 259 RIMLS, M850/2.97)

  • Shengquiang Shu

    (US Department of Energy Joint Genome Institute)

  • Joseph Carlson

    (US Department of Energy Joint Genome Institute)

  • Tsutomu Kinoshita

    (Faculty of Science, Rikkyo University)

  • Yuko Ohta

    (University of Maryland)

  • Shuuji Mawaribuchi

    (Kitasato Institute for Life Sciences, Kitasato University)

  • Jerry Jenkins

    (US Department of Energy Joint Genome Institute
    HudsonAlpha Institute of Biotechnology)

  • Jane Grimwood

    (US Department of Energy Joint Genome Institute
    HudsonAlpha Institute of Biotechnology)

  • Jeremy Schmutz

    (US Department of Energy Joint Genome Institute
    HudsonAlpha Institute of Biotechnology)

  • Therese Mitros

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Sahar V. Mozaffari

    (University of Chicago)

  • Yutaka Suzuki

    (The University of Tokyo)

  • Yoshikazu Haramoto

    (Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST))

  • Takamasa S. Yamamoto

    (National Institute for Basic Biology, 38 Nishigonaka)

  • Chiyo Takagi

    (National Institute for Basic Biology, 38 Nishigonaka)

  • Rebecca Heald

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Kelly Miller

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Christian Haudenschild

    (Illumina Inc., 25861 Industrial Blvd, Hayward
    †Present address: Personalis Inc., 1330 O’Brien Drive, Menlo Park, California 94025, USA.)

  • Jacob Kitzman

    (University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE)

  • Takuya Nakayama

    (University of Virginia)

  • Yumi Izutsu

    (Faculty of Science, Niigata University)

  • Jacques Robert

    (University of Rochester Medical Center, Rochester)

  • Joshua Fortriede

    (Cincinnati Children's Research Foundation)

  • Kevin Burns

    (Cincinnati Children's Research Foundation)

  • Vaneet Lotay

    (University of Calgary)

  • Kamran Karimi

    (University of Calgary)

  • Yuuri Yasuoka

    (Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha)

  • Darwin S. Dichmann

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Martin F. Flajnik

    (University of Maryland)

  • Douglas W. Houston

    (The University of Iowa, 257 Biology Building)

  • Jay Shendure

    (University of Washington, Foege Building S-250, Box 355065, 3720 15th Ave NE)

  • Louis DuPasquier

    (University of Basel)

  • Peter D. Vize

    (University of Calgary)

  • Aaron M. Zorn

    (Cincinnati Children's Research Foundation)

  • Michihiko Ito

    (School of Science, Kitasato University)

  • Edward M. Marcotte

    (Center for Systems and Synthetic Biology, University of Texas at Austin)

  • John B. Wallingford

    (Center for Systems and Synthetic Biology, University of Texas at Austin)

  • Yuzuru Ito

    (Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST))

  • Makoto Asashima

    (Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST))

  • Naoto Ueno

    (National Institute for Basic Biology, 38 Nishigonaka
    SOKENDAI (The Graduate University for Advanced Studies), 38 Nishigonaka, Myodaiji)

  • Yoichi Matsuda

    (Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-ku)

  • Gert Jan C. Veenstra

    (Radboud University, Faculty of Science, 259 RIMLS, M850/2.97)

  • Asao Fujiyama

    (Center for Information Biology, and Advanced Genomics Center, National Institute of Genetics
    Principles of Informatics, National Institute of Informatics, 2-1-2 Hitotsubashi
    SOKENDAI (The Graduate University for Advanced Studies))

  • Richard M. Harland

    (University of California, Berkeley, Life Sciences Addition #3200)

  • Masanori Taira

    (Graduate School of Science, The University of Tokyo)

  • Daniel S. Rokhsar

    (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)

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.

Suggested Citation

  • 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 Qu, 2016. "Genome evolution in the allotetraploid frog Xenopus laevis," Nature, Nature, vol. 538(7625), pages 336-343, October.
    • Handle: RePEc:nat:nature:v:538:y:2016:i:7625:d:10.1038_nature19840
    DOI: 10.1038/nature19840
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    Cited by:

    1. Yanting Shen & Wanying Li & Ying Zeng & Zhipeng Li & Yiqiong Chen & Jixiang Zhang & Hong Zhao & Lingfang Feng & Dongming Ma & Xiaolu Mo & Puyue Ouyang & Lili Huang & Zheng Wang & Yuannian Jiao & Hong-, 2022. "Chromosome-level and haplotype-resolved genome provides insight into the tetraploid hybrid origin of patchouli," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. John K. Barrows & Baicheng Lin & Colleen E. Quaas & George Fullbright & Elizabeth N. Wallace & David T. Long, 2022. "BRD4 promotes resection and homology-directed repair of DNA double-strand breaks," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Jessen V. Bredeson & Austin B. Mudd & Sofia Medina-Ruiz & Therese Mitros & Owen Kabnick Smith & Kelly E. Miller & Jessica B. Lyons & Sanjit S. Batra & Joseph Park & Kodiak C. Berkoff & Christopher Plo, 2024. "Conserved chromatin and repetitive patterns reveal slow genome evolution in frogs," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Camilla S. Colding-Christensen & Ellen S. Kakulidis & Javier Arroyo-Gomez & Ivo A. Hendriks & Connor Arkinson & Zita Fábián & Agnieszka Gambus & Niels Mailand & Julien P. Duxin & Michael L. Nielsen, 2023. "Profiling ubiquitin signalling with UBIMAX reveals DNA damage- and SCFβ-Trcp1-dependent ubiquitylation of the actin-organizing protein Dbn1," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Thao Nguyen & Eli J. Costa & Tim Deibert & Jose Reyes & Felix C. Keber & Miroslav Tomschik & Michael Stadlmeier & Meera Gupta & Chirag K. Kumar & Edward R. Cruz & Amanda Amodeo & Jesse C. Gatlin & Mar, 2022. "Differential nuclear import sets the timing of protein access to the embryonic genome," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Olga A. Balashova & Alexios A. Panoutsopoulos & Olesya Visina & Jacob Selhub & Paul S. Knoepfler & Laura N. Borodinsky, 2024. "Noncanonical function of folate through folate receptor 1 during neural tube formation," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Anthony K. Redmond & Dearbhaile Casey & Manu Kumar Gundappa & Daniel J. Macqueen & Aoife McLysaght, 2023. "Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Heiner Kuhl & Kang Du & Manfred Schartl & Lukáš Kalous & Matthias Stöck & Dunja K. Lamatsch, 2022. "Equilibrated evolution of the mixed auto-/allopolyploid haplotype-resolved genome of the invasive hexaploid Prussian carp," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Dadong Dai & Chuanshuai Xie & Yayi Zhou & Dexin Bo & Shurong Zhang & Shengqiang Mao & Yucheng Liao & Simeng Cui & Zhaolu Zhu & Xueyu Wang & Fanling Li & Donghai Peng & Jinshui Zheng & Ming Sun, 2023. "Unzipped chromosome-level genomes reveal allopolyploid nematode origin pattern as unreduced gamete hybridization," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. Min-Rui-Xuan Xu & Zhen-Yang Liao & Jordan R. Brock & Kang Du & Guo-Yin Li & Zhi-Qiang Chen & Ying-Hao Wang & Zhong-Nan Gao & Gaurav Agarwal & Kevin H-C Wei & Feng Shao & Shuai Pang & Adrian E. Platts , 2023. "Maternal dominance contributes to subgenome differentiation in allopolyploid fishes," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. José Cerca & Bent Petersen & José Miguel Lazaro-Guevara & Angel Rivera-Colón & Siri Birkeland & Joel Vizueta & Siyu Li & Qionghou Li & João Loureiro & Chatchai Kosawang & Patricia Jaramillo Díaz & Gon, 2022. "The genomic basis of the plant island syndrome in Darwin’s giant daisies," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    12. Adam M. Session & Daniel S. Rokhsar, 2023. "Transposon signatures of allopolyploid genome evolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    13. Johanna Klughammer & Daria Romanovskaia & Amelie Nemc & Annika Posautz & Charlotte A. Seid & Linda C. Schuster & Melissa C. Keinath & Juan Sebastian Lugo Ramos & Lindsay Kosack & Ann Evankow & Dieter , 2023. "Comparative analysis of genome-scale, base-resolution DNA methylation profiles across 580 animal species," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

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