Genome evolution in the allotetraploid frog Xenopus laevis

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 Quigley; Sven Heinz; Hajime Ogino; Haruki Ochi; Uffe Hellsten; Jessica B. Lyons; Oleg Simakov; Nicholas Putnam; Jonathan Stites; Yoko Kuroki; Toshiaki Tanaka; Tatsuo Michiue; Minoru Watanabe; Ozren Bogdanovic; Ryan Lister; Georgios Georgiou; Sarita S. Paranjpe; Ila Van Kruijsbergen; Shengquiang Shu; Joseph Carlson; Tsutomu Kinoshita; Yuko Ohta; Shuuji Mawaribuchi; Jerry Jenkins; Jane Grimwood; Jeremy Schmutz; Therese Mitros; Sahar V. Mozaffari; Yutaka Suzuki; Yoshikazu Haramoto; Takamasa S. Yamamoto; Chiyo Takagi; Rebecca Heald; Kelly Miller; Christian Haudenschild; Jacob Kitzman; Takuya Nakayama; Yumi Izutsu; Jacques Robert; Joshua Fortriede; Kevin Burns; Vaneet Lotay; Kamran Karimi; Yuuri Yasuoka; Darwin S. Dichmann; Martin F. Flajnik; Douglas W. Houston; Jay Shendure; Louis Dupasquier; Peter D. Vize; Aaron M. Zorn; Michihiko Ito; Edward M. Marcotte; John B. Wallingford; Yuzuru Ito; Makoto Asashima; Naoto Ueno; Yoichi Matsuda; Gert Jan C. Veenstra; Asao Fujiyama; Richard M. Harland; Masanori Taira; Daniel S. Rokhsar

doi:10.1038/nature19840

Genome evolution in the allotetraploid frog Xenopus laevis

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 Quigley
, Sven Heinz
, Hajime Ogino
, Haruki Ochi
, Uffe Hellsten
, Jessica B. Lyons
, Oleg Simakov
, Nicholas Putnam
, Jonathan Stites

Yoko Kuroki, Toshiaki Tanaka, Tatsuo Michiue, Minoru Watanabe, Ozren Bogdanovic, Ryan Lister, Georgios Georgiou, Sarita S. Paranjpe, Ila Van Kruijsbergen, Shengquiang Shu, Joseph Carlson, Tsutomu Kinoshita, Yuko Ohta, Shuuji Mawaribuchi, Jerry Jenkins, Jane Grimwood, Jeremy Schmutz, Therese Mitros, Sahar V. Mozaffari, Yutaka Suzuki, Yoshikazu Haramoto, Takamasa S. Yamamoto, Chiyo Takagi, Rebecca Heald, Kelly Miller, Christian Haudenschild, Jacob Kitzman, Takuya Nakayama, Yumi Izutsu, Jacques Robert, Joshua Fortriede, Kevin Burns, Vaneet Lotay, Kamran Karimi, Yuuri Yasuoka, Darwin S. Dichmann, Martin F. Flajnik, Douglas W. Houston, Jay Shendure, Louis Dupasquier, Peter D. Vize, Aaron M. Zorn, Michihiko Ito, Edward M. Marcotte, John B. Wallingford, Yuzuru Ito, Makoto Asashima, Naoto Ueno, Yoichi Matsuda, Gert Jan C. Veenstra, Asao Fujiyama, Richard M. Harland, Masanori Taira, Daniel S. Rokhsar

Biology

Binghamton University

Nagoya University
University of Texas at Austin
Ulsan National Institute of Science and Technology
United States Department of Energy
National Institute of Genetics Mishima
Hiroshima University
Hokkaido University
The University of Tokyo
Radboud University Nijmegen
Salk Institute for Biological Studies
Nagahama Institute of Bio-Science and Technology
Yamagata University
University of California at Berkeley
Okinawa Institute of Science and Technology Graduate University
Dovetail Genomics LLC.
National Center for Child Health and Development
Institute of Science Tokyo
Tokushima University
University of Western Australia
Rikkyo University
University of Maryland, Baltimore
Kitasato University
HudsonAlpha Institute for Biotechnology
The University of Chicago
National Institute of Advanced Industrial Science and Technology
National Institute for Basic Biology
Illumina, Inc.
University of Washington
University of Virginia
Niigata University
University of Rochester
Cincinnati Children's Hospital Medical Center
University of Calgary
University of Iowa
University of Basel
The Graduate University for Advanced Studies
National Institute of Informatics
Personalis Inc.

Research output: Contribution to journal › Article › peer-review

755 Scopus citations

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.

Original language	English
Pages (from-to)	336-343
Number of pages	8
Journal	Nature
Volume	538
Issue number	7625
DOIs	https://doi.org/10.1038/nature19840
State	Published - Oct 19 2016

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Session, A. M., Uno, Y., Kwon, T., Chapman, J. A., Toyoda, A., Takahashi, S., Fukui, A., Hikosaka, A., Suzuki, A., Kondo, M., Van Heeringen, S. J., Quigley, I., Heinz, S., Ogino, H., Ochi, H., Hellsten, U., Lyons, J. B., Simakov, O., Putnam, N., ... Rokhsar, D. S. (2016). Genome evolution in the allotetraploid frog Xenopus laevis. Nature, 538(7625), 336-343. https://doi.org/10.1038/nature19840

@article{7c908c9173954744bb307064e8286995,

title = "Genome evolution in the allotetraploid frog Xenopus laevis",

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.",

author = "Session, \{Adam M.\} and Yoshinobu Uno and Taejoon Kwon and Chapman, \{Jarrod A.\} and Atsushi Toyoda and Shuji Takahashi and Akimasa Fukui and Akira Hikosaka and Atsushi Suzuki and Mariko Kondo and \{Van Heeringen\}, \{Simon J.\} and Ian Quigley and Sven Heinz and Hajime Ogino and Haruki Ochi and Uffe Hellsten and Lyons, \{Jessica B.\} and Oleg Simakov and Nicholas Putnam and Jonathan Stites and Yoko Kuroki and Toshiaki Tanaka and Tatsuo Michiue and Minoru Watanabe and Ozren Bogdanovic and Ryan Lister and Georgios Georgiou and Paranjpe, \{Sarita S.\} and \{Van Kruijsbergen\}, Ila and Shengquiang Shu and Joseph Carlson and Tsutomu Kinoshita and Yuko Ohta and Shuuji Mawaribuchi and Jerry Jenkins and Jane Grimwood and Jeremy Schmutz and Therese Mitros and Mozaffari, \{Sahar V.\} and Yutaka Suzuki and Yoshikazu Haramoto and Yamamoto, \{Takamasa S.\} and Chiyo Takagi and Rebecca Heald and Kelly Miller and Christian Haudenschild and Jacob Kitzman and Takuya Nakayama and Yumi Izutsu and Jacques Robert and Joshua Fortriede and Kevin Burns and Vaneet Lotay and Kamran Karimi and Yuuri Yasuoka and Dichmann, \{Darwin S.\} and Flajnik, \{Martin F.\} and Houston, \{Douglas W.\} and Jay Shendure and Louis Dupasquier and Vize, \{Peter D.\} and Zorn, \{Aaron M.\} and Michihiko Ito and Marcotte, \{Edward M.\} and Wallingford, \{John B.\} and Yuzuru Ito and Makoto Asashima and Naoto Ueno and Yoichi Matsuda and Veenstra, \{Gert Jan C.\} and Asao Fujiyama and Harland, \{Richard M.\} and Masanori Taira and Rokhsar, \{Daniel S.\}",

note = "Publisher Copyright: {\textcopyright} 2016 The Author(s).",

year = "2016",

month = oct,

day = "19",

doi = "10.1038/nature19840",

language = "English",

volume = "538",

pages = "336--343",

journal = "Nature",

issn = "0028-0836",

number = "7625",

}

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, GJC, Fujiyama, A, Harland, RM, Taira, M & Rokhsar, DS 2016, 'Genome evolution in the allotetraploid frog Xenopus laevis', Nature, vol. 538, no. 7625, pp. 336-343. https://doi.org/10.1038/nature19840

TY - JOUR

T1 - Genome evolution in the allotetraploid frog Xenopus laevis

AU - Session, Adam M.

AU - Uno, Yoshinobu

AU - Kwon, Taejoon

AU - Chapman, Jarrod A.

AU - Toyoda, Atsushi

AU - Takahashi, Shuji

AU - Fukui, Akimasa

AU - Hikosaka, Akira

AU - Suzuki, Atsushi

AU - Kondo, Mariko

AU - Van Heeringen, Simon J.

AU - Quigley, Ian

AU - Heinz, Sven

AU - Ogino, Hajime

AU - Ochi, Haruki

AU - Hellsten, Uffe

AU - Lyons, Jessica B.

AU - Simakov, Oleg

AU - Putnam, Nicholas

AU - Stites, Jonathan

AU - Kuroki, Yoko

AU - Tanaka, Toshiaki

AU - Michiue, Tatsuo

AU - Watanabe, Minoru

AU - Bogdanovic, Ozren

AU - Lister, Ryan

AU - Georgiou, Georgios

AU - Paranjpe, Sarita S.

AU - Van Kruijsbergen, Ila

AU - Shu, Shengquiang

AU - Carlson, Joseph

AU - Kinoshita, Tsutomu

AU - Ohta, Yuko

AU - Mawaribuchi, Shuuji

AU - Jenkins, Jerry

AU - Grimwood, Jane

AU - Schmutz, Jeremy

AU - Mitros, Therese

AU - Mozaffari, Sahar V.

AU - Suzuki, Yutaka

AU - Haramoto, Yoshikazu

AU - Yamamoto, Takamasa S.

AU - Takagi, Chiyo

AU - Heald, Rebecca

AU - Miller, Kelly

AU - Haudenschild, Christian

AU - Kitzman, Jacob

AU - Nakayama, Takuya

AU - Izutsu, Yumi

AU - Robert, Jacques

AU - Fortriede, Joshua

AU - Burns, Kevin

AU - Lotay, Vaneet

AU - Karimi, Kamran

AU - Yasuoka, Yuuri

AU - Dichmann, Darwin S.

AU - Flajnik, Martin F.

AU - Houston, Douglas W.

AU - Shendure, Jay

AU - Dupasquier, Louis

AU - Vize, Peter D.

AU - Zorn, Aaron M.

AU - Ito, Michihiko

AU - Marcotte, Edward M.

AU - Wallingford, John B.

AU - Ito, Yuzuru

AU - Asashima, Makoto

AU - Ueno, Naoto

AU - Matsuda, Yoichi

AU - Veenstra, Gert Jan C.

AU - Fujiyama, Asao

AU - Harland, Richard M.

AU - Taira, Masanori

AU - Rokhsar, Daniel S.

PY - 2016/10/19

Y1 - 2016/10/19

N2 - 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.

AB - 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.

UR - https://www.scopus.com/pages/publications/84992376574

U2 - 10.1038/nature19840

DO - 10.1038/nature19840

M3 - Article

C2 - 27762356

SN - 0028-0836

VL - 538

SP - 336

EP - 343

JO - Nature

JF - Nature

IS - 7625

ER -

Genome evolution in the allotetraploid frog Xenopus laevis

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