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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
Open Access

Systems Analysis of the Response of Photosynthesis, Metabolism, and Growth to an Increase in Irradiance in the Photosynthetic Model Organism Chlamydomonas reinhardtii

Tabea Mettler, Timo Mühlhaus, Dorothea Hemme, Mark-Aurel Schöttler, Jens Rupprecht, Adam Idoine, Daniel Veyel, Sunil Kumar Pal, Liliya Yaneva-Roder, Flavia Vischi Winck, Frederik Sommer, Daniel Vosloh, Bettina Seiwert, Alexander Erban, Asdrubal Burgos, Samuel Arvidsson, Stephanie Schönfelder, Anne Arnold, Manuela Günther, Ursula Krause, Marc Lohse, Joachim Kopka, Zoran Nikoloski, Bernd Mueller-Roeber, Lothar Willmitzer, Ralph Bock, Michael Schroda, Mark Stitt
Tabea Mettler
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Timo Mühlhaus
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Dorothea Hemme
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Mark-Aurel Schöttler
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Jens Rupprecht
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Adam Idoine
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Daniel Veyel
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Sunil Kumar Pal
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Liliya Yaneva-Roder
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Flavia Vischi Winck
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
bInstitute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany
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Frederik Sommer
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Daniel Vosloh
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Bettina Seiwert
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Alexander Erban
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Asdrubal Burgos
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Samuel Arvidsson
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
bInstitute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany
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Stephanie Schönfelder
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Anne Arnold
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Manuela Günther
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Ursula Krause
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Marc Lohse
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Joachim Kopka
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Zoran Nikoloski
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Bernd Mueller-Roeber
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
bInstitute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany
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Lothar Willmitzer
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Ralph Bock
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Michael Schroda
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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Mark Stitt
aMax Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
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  • For correspondence: mstitt@mpimp-golm.mpg.de

Published June 2014. DOI: https://doi.org/10.1105/tpc.114.124537

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  • © 2014 American Society of Plant Biologists. All rights reserved.

Abstract

We investigated the systems response of metabolism and growth after an increase in irradiance in the nonsaturating range in the algal model Chlamydomonas reinhardtii. In a three-step process, photosynthesis and the levels of metabolites increased immediately, growth increased after 10 to 15 min, and transcript and protein abundance responded by 40 and 120 to 240 min, respectively. In the first phase, starch and metabolites provided a transient buffer for carbon until growth increased. This uncouples photosynthesis from growth in a fluctuating light environment. In the first and second phases, rising metabolite levels and increased polysome loading drove an increase in fluxes. Most Calvin-Benson cycle (CBC) enzymes were substrate-limited in vivo, and strikingly, many were present at higher concentrations than their substrates, explaining how rising metabolite levels stimulate CBC flux. Rubisco, fructose-1,6-biosphosphatase, and seduheptulose-1,7-bisphosphatase were close to substrate saturation in vivo, and flux was increased by posttranslational activation. In the third phase, changes in abundance of particular proteins, including increases in plastidial ATP synthase and some CBC enzymes, relieved potential bottlenecks and readjusted protein allocation between different processes. Despite reasonable overall agreement between changes in transcript and protein abundance (R2 = 0.24), many proteins, including those in photosynthesis, changed independently of transcript abundance.

  • Glossary

    CBC
    Calvin-Benson cycle
    ETR
    electron transport rate
    LC-MS/MS
    liquid chromatography–tandem mass spectrometry
    GC-MS
    gas chromatography–mass spectrometry
    PC
    principle component
    TCA
    tricarboxylic acid
    ATPase
    ATP synthase
    MGDG
    monogalactosyldiacylglycerol
    DGTS
    diacylglycerol-N,N,N-trimethylhomoserine
    DGDG
    digalactosyldiacylglycerol
    TAG
    triacylglycerol
    emPAI
    exponentially modified protein abundance index
    RA
    relative abundance
    UPLC
    ultraperformance liquid chromatography
    • Received February 23, 2014.
    • Revised April 17, 2014.
    • Accepted May 6, 2014.
    • Published June 3, 2014.

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    Systems Analysis of the Response of Photosynthesis, Metabolism, and Growth to an Increase in Irradiance in the Photosynthetic Model Organism Chlamydomonas reinhardtii
    Tabea Mettler, Timo Mühlhaus, Dorothea Hemme, Mark-Aurel Schöttler, Jens Rupprecht, Adam Idoine, Daniel Veyel, Sunil Kumar Pal, Liliya Yaneva-Roder, Flavia Vischi Winck, Frederik Sommer, Daniel Vosloh, Bettina Seiwert, Alexander Erban, Asdrubal Burgos, Samuel Arvidsson, Stephanie Schönfelder, Anne Arnold, Manuela Günther, Ursula Krause, Marc Lohse, Joachim Kopka, Zoran Nikoloski, Bernd Mueller-Roeber, Lothar Willmitzer, Ralph Bock, Michael Schroda, Mark Stitt
    The Plant Cell Jun 2014, 26 (6) 2310-2350; DOI: 10.1105/tpc.114.124537

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    Systems Analysis of the Response of Photosynthesis, Metabolism, and Growth to an Increase in Irradiance in the Photosynthetic Model Organism Chlamydomonas reinhardtii
    Tabea Mettler, Timo Mühlhaus, Dorothea Hemme, Mark-Aurel Schöttler, Jens Rupprecht, Adam Idoine, Daniel Veyel, Sunil Kumar Pal, Liliya Yaneva-Roder, Flavia Vischi Winck, Frederik Sommer, Daniel Vosloh, Bettina Seiwert, Alexander Erban, Asdrubal Burgos, Samuel Arvidsson, Stephanie Schönfelder, Anne Arnold, Manuela Günther, Ursula Krause, Marc Lohse, Joachim Kopka, Zoran Nikoloski, Bernd Mueller-Roeber, Lothar Willmitzer, Ralph Bock, Michael Schroda, Mark Stitt
    The Plant Cell Jun 2014, 26 (6) 2310-2350; DOI: 10.1105/tpc.114.124537
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