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, L.I.A.C. Villalobos, John M. Clay, Roman Skokan & 40 others 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

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

57 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)448-464.e24
JournalCell
Volume174
Issue number2
DOIs
Publication statusPublished - 12 Jul 2018

Fingerprint

Chara
Embryophyta
Genes
Genome
Charophyceae
Algae
Reactive Oxygen Species
Transcription Factors
Plant Genes
Plastids
Plant Growth Regulators
Cell Separation
Zygote
Gene Regulatory Networks
Heat-Shock Proteins
Biosynthesis
Cell Wall
Phosphotransferases
Cells

Keywords

  • Chara
  • charophyte
  • phragmoplast
  • Phragmoplastophyta
  • phytohormones
  • plant evolution
  • reactive oxygen species
  • streptophyte
  • transcriptional regulation

Cite this

Nishiyama, T., Sakayama, H., de Vries, J., Buschmann, H., Saint-Marcoux, D., Ullrich, K. K., ... Rensing, S. A. (2018). The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization. Cell, 174(2), 448-464.e24. https://doi.org/10.1016/j.cell.2018.06.033
Nishiyama, Tomoaki ; Sakayama, Hidetoshi ; de Vries, Jan ; Buschmann, Henrik ; Saint-Marcoux, Denis ; Ullrich, Kristian K. ; Haas, Fabian B. ; Vanderstraeten, Lisa ; Becker, Dirk ; Lang, Daniel ; Vosolsobě, Stanislav ; Rombauts, Stephane ; Wilhelmsson, Per K.I. ; Janitza, Philipp ; Kern, Ramona ; Heyl, Alexander ; Rümpler, Florian ; Villalobos, L.I.A.C. ; Clay, John M. ; Skokan, Roman ; Toyoda, Atsushi ; Suzuki, Yutaka ; Kagoshima, Hiroshi ; Schijlen, Elio ; Tajeshwar, Navindra ; Catarino, Bruno ; Hetherington, Alexander J. ; Saltykova, Assia ; Bonnot, Clemence ; Breuninger, Holger ; Symeonidi, Aikaterini ; Radhakrishnan, Guru V. ; Van Nieuwerburgh, Filip ; Deforce, Dieter ; Chang, Caren ; Karol, Kenneth G. ; Hedrich, Rainer ; Ulvskov, Peter ; Glöckner, Gernot ; Delwiche, Charles F. ; Petrášek, Jan ; Van de Peer, Yves ; Friml, Jiri ; Beilby, Mary ; Dolan, Liam ; Kohara, Yuji ; Sugano, Sumio ; Fujiyama, Asao ; Delaux, Pierre Marc ; Quint, Marcel ; Theißen, Günter ; Hagemann, Martin ; Harholt, Jesper ; Dunand, Christophe ; Zachgo, Sabine ; Langdale, Jane ; Maumus, Florian ; Van Der Straeten, Dominique ; Gould, Sven B. ; Rensing, Stefan A. / The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization. In: Cell. 2018 ; Vol. 174, No. 2. pp. 448-464.e24.
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title = "The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization",
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, charophyte, phragmoplast, Phragmoplastophyta, phytohormones, plant evolution, reactive oxygen species, streptophyte, transcriptional regulation",
author = "Tomoaki Nishiyama and Hidetoshi Sakayama and {de Vries}, Jan and Henrik Buschmann and Denis Saint-Marcoux and Ullrich, {Kristian K.} and Haas, {Fabian B.} and Lisa Vanderstraeten and Dirk Becker and Daniel Lang and Stanislav Vosolsobě and Stephane Rombauts and Wilhelmsson, {Per K.I.} and Philipp Janitza and Ramona Kern and Alexander Heyl and Florian R{\"u}mpler and L.I.A.C. Villalobos and Clay, {John M.} and Roman Skokan and Atsushi Toyoda and Yutaka Suzuki and Hiroshi Kagoshima and Elio Schijlen and Navindra Tajeshwar and Bruno Catarino and Hetherington, {Alexander J.} and Assia Saltykova and Clemence Bonnot and Holger Breuninger and Aikaterini Symeonidi and Radhakrishnan, {Guru V.} and {Van Nieuwerburgh}, Filip and Dieter Deforce and Caren Chang and Karol, {Kenneth G.} and Rainer Hedrich and Peter Ulvskov and Gernot Gl{\"o}ckner and Delwiche, {Charles F.} and Jan Petr{\'a}šek and {Van de Peer}, Yves and Jiri Friml and Mary Beilby and Liam Dolan and Yuji Kohara and Sumio Sugano and Asao Fujiyama and Delaux, {Pierre Marc} and Marcel Quint and G{\"u}nter Thei{\ss}en and Martin Hagemann and Jesper Harholt and Christophe Dunand and Sabine Zachgo and Jane Langdale and Florian Maumus and {Van Der Straeten}, Dominique and Gould, {Sven B.} and Rensing, {Stefan A.}",
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Nishiyama, T, Sakayama, H, de Vries, J, Buschmann, H, Saint-Marcoux, D, Ullrich, KK, Haas, FB, Vanderstraeten, L, Becker, D, Lang, D, Vosolsobě, S, Rombauts, S, Wilhelmsson, PKI, Janitza, P, Kern, R, Heyl, A, Rümpler, F, Villalobos, LIAC, Clay, JM, Skokan, R, Toyoda, A, Suzuki, Y, Kagoshima, H, Schijlen, E, Tajeshwar, N, Catarino, B, Hetherington, AJ, Saltykova, A, Bonnot, C, Breuninger, H, Symeonidi, A, Radhakrishnan, GV, Van Nieuwerburgh, F, Deforce, D, Chang, C, Karol, KG, Hedrich, R, Ulvskov, P, Glöckner, G, Delwiche, CF, Petrášek, J, Van de Peer, Y, Friml, J, Beilby, M, Dolan, L, Kohara, Y, Sugano, S, Fujiyama, A, Delaux, PM, Quint, M, Theißen, G, Hagemann, M, Harholt, J, Dunand, C, Zachgo, S, Langdale, J, Maumus, F, Van Der Straeten, D, Gould, SB & Rensing, SA 2018, 'The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization', Cell, vol. 174, no. 2, pp. 448-464.e24. https://doi.org/10.1016/j.cell.2018.06.033

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

In: Cell, Vol. 174, No. 2, 12.07.2018, p. 448-464.e24.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization

AU - Nishiyama, Tomoaki

AU - Sakayama, Hidetoshi

AU - de Vries, Jan

AU - Buschmann, Henrik

AU - Saint-Marcoux, Denis

AU - Ullrich, Kristian K.

AU - Haas, Fabian B.

AU - Vanderstraeten, Lisa

AU - Becker, Dirk

AU - Lang, Daniel

AU - Vosolsobě, Stanislav

AU - Rombauts, Stephane

AU - Wilhelmsson, Per K.I.

AU - Janitza, Philipp

AU - Kern, Ramona

AU - Heyl, Alexander

AU - Rümpler, Florian

AU - Villalobos, L.I.A.C.

AU - Clay, John M.

AU - Skokan, Roman

AU - Toyoda, Atsushi

AU - Suzuki, Yutaka

AU - Kagoshima, Hiroshi

AU - Schijlen, Elio

AU - Tajeshwar, Navindra

AU - Catarino, Bruno

AU - Hetherington, Alexander J.

AU - Saltykova, Assia

AU - Bonnot, Clemence

AU - Breuninger, Holger

AU - Symeonidi, Aikaterini

AU - Radhakrishnan, Guru V.

AU - Van Nieuwerburgh, Filip

AU - Deforce, Dieter

AU - Chang, Caren

AU - Karol, Kenneth G.

AU - Hedrich, Rainer

AU - Ulvskov, Peter

AU - Glöckner, Gernot

AU - Delwiche, Charles F.

AU - Petrášek, Jan

AU - Van de Peer, Yves

AU - Friml, Jiri

AU - Beilby, Mary

AU - Dolan, Liam

AU - Kohara, Yuji

AU - Sugano, Sumio

AU - Fujiyama, Asao

AU - Delaux, Pierre Marc

AU - Quint, Marcel

AU - Theißen, Günter

AU - Hagemann, Martin

AU - Harholt, Jesper

AU - Dunand, Christophe

AU - Zachgo, Sabine

AU - Langdale, Jane

AU - Maumus, Florian

AU - Van Der Straeten, Dominique

AU - Gould, Sven B.

AU - Rensing, Stefan A.

PY - 2018/7/12

Y1 - 2018/7/12

N2 - 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.

AB - 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.

KW - Chara

KW - charophyte

KW - phragmoplast

KW - Phragmoplastophyta

KW - phytohormones

KW - plant evolution

KW - reactive oxygen species

KW - streptophyte

KW - transcriptional regulation

U2 - 10.1016/j.cell.2018.06.033

DO - 10.1016/j.cell.2018.06.033

M3 - Article

VL - 174

SP - 448-464.e24

JO - Cell

JF - Cell

SN - 0092-8674

IS - 2

ER -

Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D, Ullrich KK et al. The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization. Cell. 2018 Jul 12;174(2):448-464.e24. https://doi.org/10.1016/j.cell.2018.06.033