Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

John L Bowman; Takayuki Kohchi; Katsuyuki T Yamato; Jerry Jenkins; Shengqiang Shu; Kimitsune Ishizaki; Shohei Yamaoka; Ryuichi Nishihama; Yasukazu Nakamura; Frédéric Berger; Catherine Adam; Shiori Sugamata Aki; Felix Althoff; Takashi Araki; Mario A Arteaga-Vazquez; Sureshkumar Balasubrmanian; Kerrie Barry; Diane Bauer; Christian R Boehm; Liam Briginshaw; Juan Caballero-Perez; Bruno Catarino; Feng Chen; Shota Chiyoda; Mansi Chovatia; Kevin M Davies; Mihails Delmans; Taku Demura; Tom Dierschke; Liam Dolan; Ana E Dorantes-Acosta; D Magnus Eklund; Stevie N Florent; Eduardo Flores-Sandoval; Asao Fujiyama; Hideya Fukuzawa; Bence Galik; Daniel Grimanelli; Jane Grimwood; Ueli Grossniklaus; Takahiro Hamada; Jim Haseloff; Alexander J Hetherington; Asuka Higo; Yuki Hirakawa; Hope N Hundley; Yoko Ikeda; Keisuke Inoue; Shin-Ichiro Inoue; Sakiko Ishida; Qidong Jia; Mitsuru Kakita; Takehiko Kanazawa; Yosuke Kawai; Tomokazu Kawashima; Megan Kennedy; Keita Kinose; Toshinori Kinoshita; Yuji Kohara; Eri Koide; Kenji Komatsu; Sarah Kopischke; Minoru Kubo; Junko Kyozuka; Ulf Lagercrantz; Shih-Shun Lin; Erika Lindquist; Anna M Lipzen; Chia-Wei Lu; Efraín De Luna; Robert A Martienssen; Naoki Minamino; Masaharu Mizutani; Miya Mizutani; Nobuyoshi Mochizuki; Isabel Monte; Rebecca Mosher; Hideki Nagasaki; Hirofumi Nakagami; Satoshi Naramoto; Kazuhiko Nishitani; Misato Ohtani; Takashi Okamoto; Masaki Okumura; Jeremy Phillips; Bernardo Pollak; Anke Reinders; Moritz Rövekamp; Ryosuke Sano; Shinichiro Sawa; Marc W Schmid; Makoto Shirakawa; Roberto Solano; Alexander Spunde; Noriyuki Suetsugu; Sumio Sugano; Akifumi Sugiyama; Rui Sun; Yutaka Suzuki; Mizuki Takenaka; Daisuke Takezawa; Hirokazu Tomogane; Masayuki Tsuzuki; Takashi Ueda; Masaaki Umeda; John M Ward; Yuichiro Watanabe; Kazufumi Yazaki; Ryusuke Yokoyama; Yoshihiro Yoshitake; Izumi Yotsui; Sabine Zachgo; Jeremy Schmutz

doi:10.1016/j.cell.2017.09.030

Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

Cell. 2017 Oct 5;171(2):287-304.e15. doi: 10.1016/j.cell.2017.09.030.

Authors

John L Bowman¹, Takayuki Kohchi², Katsuyuki T Yamato³, Jerry Jenkins⁴, Shengqiang Shu⁵, Kimitsune Ishizaki⁶, Shohei Yamaoka⁷, Ryuichi Nishihama⁷, Yasukazu Nakamura⁸, Frédéric Berger⁹, Catherine Adam⁵, Shiori Sugamata Aki¹⁰, Felix Althoff¹¹, Takashi Araki⁷, Mario A Arteaga-Vazquez¹², Sureshkumar Balasubrmanian¹³, Kerrie Barry⁵, Diane Bauer⁵, Christian R Boehm¹⁴, Liam Briginshaw¹³, Juan Caballero-Perez¹⁵, Bruno Catarino¹⁶, Feng Chen¹⁷, Shota Chiyoda⁷, Mansi Chovatia⁵, Kevin M Davies¹⁸, Mihails Delmans¹⁴, Taku Demura¹⁰, Tom Dierschke¹⁹, Liam Dolan¹⁶, Ana E Dorantes-Acosta¹², D Magnus Eklund²⁰, Stevie N Florent¹³, Eduardo Flores-Sandoval¹³, Asao Fujiyama⁸, Hideya Fukuzawa⁷, Bence Galik²¹, Daniel Grimanelli²², Jane Grimwood⁴, Ueli Grossniklaus²³, Takahiro Hamada²⁴, Jim Haseloff¹⁴, Alexander J Hetherington¹⁶, Asuka Higo⁷, Yuki Hirakawa²⁵, Hope N Hundley⁵, Yoko Ikeda²⁶, Keisuke Inoue⁷, Shin-Ichiro Inoue²⁷, Sakiko Ishida⁷, Qidong Jia¹⁷, Mitsuru Kakita²⁷, Takehiko Kanazawa²⁸, Yosuke Kawai²⁹, Tomokazu Kawashima³⁰, Megan Kennedy⁵, Keita Kinose⁷, Toshinori Kinoshita³¹, Yuji Kohara⁸, Eri Koide⁷, Kenji Komatsu³², Sarah Kopischke¹¹, Minoru Kubo¹⁰, Junko Kyozuka³³, Ulf Lagercrantz³⁴, Shih-Shun Lin³⁵, Erika Lindquist⁵, Anna M Lipzen⁵, Chia-Wei Lu³⁵, Efraín De Luna³⁶, Robert A Martienssen³⁷, Naoki Minamino²⁸, Masaharu Mizutani³⁸, Miya Mizutani⁷, Nobuyoshi Mochizuki³⁹, Isabel Monte⁴⁰, Rebecca Mosher⁴¹, Hideki Nagasaki⁴², Hirofumi Nakagami⁴³, Satoshi Naramoto³³, Kazuhiko Nishitani⁴⁴, Misato Ohtani¹⁰, Takashi Okamoto⁴⁵, Masaki Okumura²⁷, Jeremy Phillips⁵, Bernardo Pollak¹⁴, Anke Reinders⁴⁶, Moritz Rövekamp²³, Ryosuke Sano¹⁰, Shinichiro Sawa⁴⁷, Marc W Schmid²³, Makoto Shirakawa⁷, Roberto Solano⁴⁰, Alexander Spunde⁵, Noriyuki Suetsugu⁷, Sumio Sugano⁴⁸, Akifumi Sugiyama⁴⁹, Rui Sun⁷, Yutaka Suzuki⁴⁸, Mizuki Takenaka⁵⁰, Daisuke Takezawa⁵¹, Hirokazu Tomogane⁷, Masayuki Tsuzuki²⁴, Takashi Ueda⁵², Masaaki Umeda¹⁰, John M Ward⁴⁶, Yuichiro Watanabe²⁴, Kazufumi Yazaki⁴⁹, Ryusuke Yokoyama⁴⁴, Yoshihiro Yoshitake⁷, Izumi Yotsui⁵³, Sabine Zachgo¹¹, Jeremy Schmutz⁴

Affiliations

¹ School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia. Electronic address: john.bowman@monash.edu.
² Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan. Electronic address: tkohchi@lif.kyoto-u.ac.jp.
³ Faculty of Biology-Oriented Science and Technology, Kindai University, 930 Nishimitani, Kinokawa, Wakayama 649-6493, Japan. Electronic address: kyamato@waka.kindai.ac.jp.
⁴ Department of Energy Joint Genome Institute, Walnut Creek, CA, USA; HudsonAlpha Institute of Biotechnology, Huntsville, AL, USA.
⁵ Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
⁶ Graduate School of Science, Kobe University, Kobe 657-8501, Japan.
⁷ Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan.
⁸ National Institute of Genetics, Research Organization of Information and Systems, Yata, Mishima 411-8540, Japan.
⁹ Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria.
¹⁰ Graduate School of Biological Sciences, Nara Institute of Science and Technology, Takayama 8916-5, Ikoma, Nara 630-0192, Japan.
¹¹ Botany Department, University of Osnabrück, Barbarastr. 11, D-49076 Osnabrück, Germany.
¹² Universidad Veracruzana, INBIOTECA - Instituto de Biotecnología y Ecología Aplicada, Av. de las Culturas Veracruzanas No.101, Colonia Emiliano Zapata, 91090, Xalapa, Veracruz, México.
¹³ School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia.
¹⁴ Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, United Kingdom.
¹⁵ National Laboratory of Genomics for Biodiversity, CINVESTAV-IPN, Km 9.6 Lib. Norte Carr. Irapuato-León, 36821, Irapuato, Guanajuato, México.
¹⁶ Department of Plant Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK.
¹⁷ Department of Plant Sciences, University of Tennessee, Knoxville, TN, USA.
¹⁸ The New Zealand Institute for Plant & Food Research Limited, Private Bag 11-600, Palmerston North, New Zealand.
¹⁹ School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia; Botany Department, University of Osnabrück, Barbarastr. 11, D-49076 Osnabrück, Germany.
²⁰ School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia; Department of Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-75236 Uppsala, Sweden.
²¹ Bioinformatics & Scientific Computing, Vienna Biocenter Core Facilities (VBCF), Dr. Bohr-Gasse 3, 1030 Vienna, Austria.
²² Institut de Recherche pour le Développement (IRD), UMR232, Université de Montpellier, Montpellier 34394, France.
²³ Department of Plant and Microbial Biology and Zurich-Basel Plant Science Center, University of Zurich, 8008 Zürich, Switzerland.
²⁴ Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo 153-8902 Japan.
²⁵ School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia; Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan; Department of Life Science, Faculty of Science, Gakushuin University, Tokyo 171-8588, Japan.
²⁶ Institute of Plant Science and Resources, Okayama University, Chuo 2-20-1, Kurashiki, Okayama 710-0046, Japan.
²⁷ Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa, Nagoya 464-8602, Japan.
²⁸ National Institute for Basic Biology, 38 Nishigounaka, Myodaiji, Okazaki 444-8585, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.
²⁹ Department of Integrative Genomics, Tohoku Medical Bank Organization, Tohoku University, Aoba, Sendai 980-8573, Japan.
³⁰ Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Dr. Bohr-Gasse 3, 1030 Vienna, Austria; Department of Plant and Soil Sciences, University of Kentucky, 321 Plant Science Building, 1405 Veterans Dr., Lexington, KY 40546, USA.
³¹ Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan; Department of Life Science, Faculty of Science, Gakushuin University, Tokyo 171-8588, Japan; Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa, Nagoya 464-8602, Japan.
³² Department of Bioproduction Technology, Junior College of Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan.
³³ Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, Japan.
³⁴ Department of Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-75236 Uppsala, Sweden.
³⁵ Institute of Biotechnology, National Taiwan University, Taipei, Taiwan.
³⁶ Instituto de Ecología, AC., Red de Biodiversidad y Sistemática, Xalapa, Veracruz, 91000, México.
³⁷ Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY, USA.
³⁸ Graduate School of Agricultural Science, Kobe University, Rokkodai, Nada, Kobe 657-8501, Japan.
³⁹ Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.
⁴⁰ Department Genética Molecular de Plantas, Centro Nacional de Biotecnologia-CSIC, Universidad Autónoma de Madrid 28049 Madrid. Spain.
⁴¹ The School of Plant Sciences, The University of Arizona, Tuscon, AZ, USA.
⁴² National Institute of Genetics, Research Organization of Information and Systems, Yata, Mishima 411-8540, Japan; Department of Technology Development, Kazusa DNA Research Institute, Kisarazu, Chiba 292-0818, Japan.
⁴³ RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan; Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany.
⁴⁴ Laboratory of Plant Cell Wall Biology, Graduate School of Life Sciences, Tohoku University, Aoba, Sendai 980-8578, Japan.
⁴⁵ Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan.
⁴⁶ Department of Plant and Microbial Biology, University of Minnesota, St. Paul, MN, USA.
⁴⁷ Graduate school of Science and Technology, Kumamoto University, Kurokami 2-39-1, Kumamoto 860-8555, Japan.
⁴⁸ Department of Computational Biology and Medical Sciences, the University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8562 Japan.
⁴⁹ Research Institute for Sustainable Humanosphere, Kyoto University, Gokasho, Uji 611-0011, Japan.
⁵⁰ Molekulare Botanik, Universität Ulm, 89069 Ulm, Germany.
⁵¹ Graduate School of Science and Engineering and Institute for Environmental Science and Technology, Saitama University, Saitama 338-8570, Japan.
⁵² National Institute for Basic Biology, 38 Nishigounaka, Myodaiji, Okazaki 444-8585, Japan.
⁵³ RIKEN Center for Sustainable Resource Science, Yokohama 230-0045, Japan.

PMID: 28985561
DOI: 10.1016/j.cell.2017.09.030

Abstract

The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PAPERCLIP.

Keywords: Marchantia polymorpha; auxin; charophycean algae; land plant evolution; sex chromosome.

MeSH terms

Adaptation, Biological
Biological Evolution*
Embryophyta / genetics*
Embryophyta / physiology
Gene Expression Regulation, Plant
Genome, Plant*
Marchantia / genetics*
Marchantia / physiology
Molecular Sequence Annotation
Signal Transduction
Transcription, Genetic

Abstract

MeSH terms

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