The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization

Tomoaki Nishiyama; Hidetoshi Sakayama; Jan de Vries; Henrik Buschmann; Denis Saint-Marcoux; Kristian K Ullrich; Fabian B Haas; Lisa Vanderstraeten; Dirk Becker; Daniel Lang; Stanislav Vosolsobě; Stephane Rombauts; Per K I Wilhelmsson; Philipp Janitza; Ramona Kern; Alexander Heyl; Florian Rümpler; Luz Irina A Calderón Villalobos; John M Clay; Roman Skokan; Atsushi Toyoda; Yutaka Suzuki; Hiroshi Kagoshima; Elio Schijlen; Navindra Tajeshwar; Bruno Catarino; Alexander J Hetherington; Assia Saltykova; Clemence Bonnot; Holger Breuninger; Aikaterini Symeonidi; Guru V Radhakrishnan; Filip Van Nieuwerburgh; Dieter Deforce; Caren Chang; Kenneth G Karol; Rainer Hedrich; Peter Ulvskov; Gernot Glöckner; Charles F Delwiche; Jan Petrášek; Yves Van de Peer; Jiri Friml; Mary Beilby; Liam Dolan; Yuji Kohara; Sumio Sugano; Asao Fujiyama; Pierre-Marc Delaux; Marcel Quint; Günter Theißen; Martin Hagemann; Jesper Harholt; Christophe Dunand; Sabine Zachgo; Jane Langdale; Florian Maumus; Dominique Van Der Straeten; Sven B Gould; Stefan A Rensing

doi:10.1016/j.cell.2018.06.033

The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization

Cell. 2018 Jul 12;174(2):448-464.e24. doi: 10.1016/j.cell.2018.06.033.

Authors

Tomoaki Nishiyama¹, Hidetoshi Sakayama², Jan de Vries³, Henrik Buschmann⁴, Denis Saint-Marcoux⁵, Kristian K Ullrich⁶, Fabian B Haas⁶, Lisa Vanderstraeten⁷, Dirk Becker⁸, Daniel Lang⁹, Stanislav Vosolsobě¹⁰, Stephane Rombauts¹¹, Per K I Wilhelmsson⁶, Philipp Janitza¹², Ramona Kern¹³, Alexander Heyl¹⁴, Florian Rümpler¹⁵, Luz Irina A Calderón Villalobos¹⁶, John M Clay¹⁷, Roman Skokan¹⁰, Atsushi Toyoda¹⁸, Yutaka Suzuki¹⁹, Hiroshi Kagoshima²⁰, Elio Schijlen²¹, Navindra Tajeshwar¹⁴, Bruno Catarino²², Alexander J Hetherington²², Assia Saltykova²³, Clemence Bonnot²², Holger Breuninger²⁴, Aikaterini Symeonidi⁶, Guru V Radhakrishnan²⁵, Filip Van Nieuwerburgh²⁶, Dieter Deforce²⁶, Caren Chang¹⁷, Kenneth G Karol²⁷, Rainer Hedrich⁸, Peter Ulvskov²⁸, Gernot Glöckner²⁹, Charles F Delwiche¹⁷, Jan Petrášek¹⁰, Yves Van de Peer³⁰, Jiri Friml³¹, Mary Beilby³², Liam Dolan²², Yuji Kohara²⁰, Sumio Sugano¹⁹, Asao Fujiyama¹⁸, Pierre-Marc Delaux³³, Marcel Quint³⁴, Günter Theißen¹⁵, Martin Hagemann¹³, Jesper Harholt³⁵, Christophe Dunand³³, Sabine Zachgo⁴, Jane Langdale²², Florian Maumus³⁶, Dominique Van Der Straeten⁷, Sven B Gould³⁷, Stefan A Rensing³⁸

Affiliations

¹ Advanced Science Research Center, Kanazawa University, Kanazawa 920-0934, Japan. Electronic address: tomoakin@staff.kanazawa-u.ac.jp.
² Graduate School of Science, Kobe University, Kobe 657-8501, Japan. Electronic address: hsak@port.kobe-u.ac.jp.
³ Institute for Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany; Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada.
⁴ Botany Department, School of Biology and Chemistry, Osnabrück University, 49076 Osnabrück, Germany.
⁵ Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK; Université de Lyon, UJM-Saint-Étienne, CNRS, BVpam FRE3727, 42023 Saint-Étienne, France.
⁶ Plant Cell Biology, Faculty of Biology, University of Marburg, 35043 Marburg, Germany.
⁷ Laboratory of Functional Plant Biology, Department of Biology, Gent University, 9000 Gent, Belgium.
⁸ Molecular Plant Physiology & Biophysics, University of Wuerzburg, 97082 Wuerzburg, Germany.
⁹ PGSB, Helmholtz Center Munich, 85764 Neuherberg, Germany.
¹⁰ Department of Experimental Plant Biology, Faculty of Science, Charles University, 128 44 Prague 2, Czech Republic.
¹¹ Department of Plant Biotechnology and Bioinformatics, Gent University and VIB Center for Plant Systems Biology, 9052 Gent, Belgium.
¹² Institute of Agricultural and Nutritional Sciences, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany.
¹³ Plant Physiology, University Rostock, 18051 Rostock, Germany.
¹⁴ Department of Biology, Adelphi University, Garden City, NY 11530, USA.
¹⁵ Department of Genetics, Friedrich Schiller University Jena, 07743 Jena, Germany.
¹⁶ Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany.
¹⁷ CBMG, University of Maryland, College Park, MD 20742, USA.
¹⁸ Comparative Genomics Laboratory and Advanced Genomics Center, National Institute of Genetics, Shizuoka 411-8540, Japan.
¹⁹ Department of Computational Biology and Medical Sciences, University of Tokyo, Kashiwa, Chiba 277-8562, Japan.
²⁰ Genome Biology Laboratory, National Institute of Genetics, Shizuoka 411-8540, Japan.
²¹ Wageningen University, B.U. Bioscience, 6700 AA Wageningen, the Netherlands.
²² Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK.
²³ Department of Plant Biotechnology and Bioinformatics, Gent University and VIB Center for Plant Systems Biology, 9052 Gent, Belgium; Platform Biotechnology and Molecular Biology, Scientific Institute of Public Health (WIV-ISP), Brussels, Belgium; Department of Information Technology, Gent University, IMinds, 9052 Gent, Belgium.
²⁴ Department of Plant Sciences, University of Oxford, Oxford OX1 3RB, UK; ZMBP, Entwicklungsgenetik, 72076 Tübingen, Germany.
²⁵ Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, United Kingdom.
²⁶ Laboratory of Pharmaceutical Biotechnology, Gent University, 9000 Gent, Belgium.
²⁷ Lewis B. and Dorothy Cullman Program for Molecular Systematics, The New York Botanical Garden, Bronx, NY 10458, USA.
²⁸ Department of Plant and Environmental Sciences, University of Copenhagen, DK-1871 Frederiksberg C, Denmark.
²⁹ Biochemistry I, Medical Faculty, University of Cologne, 50931 Cologne, Germany.
³⁰ Department of Plant Biotechnology and Bioinformatics, Gent University and VIB Center for Plant Systems Biology, 9052 Gent, Belgium; Department of Biochemistry, Genetics and Microbiology, University of Pretoria, Pretoria 0028, South Africa.
³¹ Institute of Science and Technology, 3400 Klosterneuburg, Austria.
³² School of Physics, University of NSW, Sydney, Kensington, 2052 NSW, Australia.
³³ Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, CNRS, UPS, Auzeville, BP42617, 31326 Castanet Tolosan, France.
³⁴ Institute of Agricultural and Nutritional Sciences, Martin Luther University Halle-Wittenberg, 06120 Halle (Saale), Germany; Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany.
³⁵ Carlsberg Research Laboratory, 1799 Copenhagen V, Denmark.
³⁶ URGI, INRA, Université Paris-Saclay, 78026 Versailles, France.
³⁷ Institute for Molecular Evolution, Heinrich Heine University, 40225 Düsseldorf, Germany.
³⁸ Plant Cell Biology, Faculty of Biology, University of Marburg, 35043 Marburg, Germany; BIOSS Centre for Biological Signalling Studies, Unigersity Freiburg, Germany. Electronic address: stefan.rensing@biologie.uni-marburg.de.

PMID: 30007417
DOI: 10.1016/j.cell.2018.06.033

Abstract

Land plants evolved from charophytic algae, among which Charophyceae possess the most complex body plans. We present the genome of Chara braunii; comparison of the genome to those of land plants identified evolutionary novelties for plant terrestrialization and land plant heritage genes. C. braunii employs unique xylan synthases for cell wall biosynthesis, a phragmoplast (cell separation) mechanism similar to that of land plants, and many phytohormones. C. braunii plastids are controlled via land-plant-like retrograde signaling, and transcriptional regulation is more elaborate than in other algae. The morphological complexity of this organism may result from expanded gene families, with three cases of particular note: genes effecting tolerance to reactive oxygen species (ROS), LysM receptor-like kinases, and transcription factors (TFs). Transcriptomic analysis of sexual reproductive structures reveals intricate control by TFs, activity of the ROS gene network, and the ancestral use of plant-like storage and stress protection proteins in the zygote.

Keywords: Chara; Phragmoplastophyta; charophyte; phragmoplast; phytohormones; plant evolution; reactive oxygen species; streptophyte; transcriptional regulation.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Biological Evolution
Cell Wall / metabolism
Chara / genetics*
Chara / growth & development
Embryophyta / genetics
Gene Regulatory Networks
Genome, Plant*
Pentosyltransferases / genetics
Plant Growth Regulators / metabolism
Plant Proteins / genetics
Plant Proteins / metabolism
Protein Serine-Threonine Kinases / genetics
Protein Serine-Threonine Kinases / metabolism
Reactive Oxygen Species / metabolism
Transcription Factors / genetics
Transcription Factors / metabolism
Transcriptome

Substances

Plant Growth Regulators
Plant Proteins
Reactive Oxygen Species
Transcription Factors
Pentosyltransferases
1,4-beta-D-xylan synthase
Protein Serine-Threonine Kinases