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  • Molecular Systems Biology: 14 (3)

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Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism

View ORCID ProfileDaniel D Seaton, View ORCID ProfileAlexander Graf, View ORCID ProfileKatja Baerenfaller, View ORCID ProfileMark Stitt, View ORCID ProfileAndrew J Millar, View ORCID ProfileWilhelm Gruissem
DOI 10.15252/msb.20177962 | Published online 01.03.2018
Molecular Systems Biology (2018) 14, e7962
Daniel D Seaton
SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh, UK
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Alexander Graf
Department of Biology, Institute of Molecular Plant Biology, ETH Zurich, Zurich, Switzerland
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Katja Baerenfaller
Department of Biology, Institute of Molecular Plant Biology, ETH Zurich, Zurich, Switzerland
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Mark Stitt
System Regulation Group, Max Planck Institute of Molecular Plant Physiology, Potsdam‐Golm, Germany
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Andrew J Millar
SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh, UK
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Wilhelm Gruissem
Department of Biology, Institute of Molecular Plant Biology, ETH Zurich, Zurich, Switzerland
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Author Affiliations

  1. Daniel D Seaton1,4,†,
  2. Alexander Graf2,5,†,
  3. Katja Baerenfaller2,6,
  4. Mark Stitt3,
  5. Andrew J Millar (andrew.millar{at}ed.ac.uk)*,1 and
  6. Wilhelm Gruissem (wgruisse{at}ethz.ch)*,2
  1. 1SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh, UK
  2. 2Department of Biology, Institute of Molecular Plant Biology, ETH Zurich, Zurich, Switzerland
  3. 3System Regulation Group, Max Planck Institute of Molecular Plant Physiology, Potsdam‐Golm, Germany
  4. 4Present Address: European Molecular Biology Laboratory, European Bioinformatics Institute, Hinxton, UK
  5. 5Present Address: Plant Proteomics Group, Max Planck Institute of Molecular Plant Physiology, Potsdam‐Golm, Germany
  6. 6Present Address: Swiss Institute of Allergy and Asthma Research, University of Zürich, Davos, Switzerland
  1. ↵* Corresponding author. Tel: +44 131 651 3325; Email: andrew.millar{at}ed.ac.uk
    Corresponding author. Tel: +41 44 632 0857; Email: wgruisse{at}ethz.ch
  1. ↵† These authors contributed equally to this work

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Abstract

Plants respond to seasonal cues such as the photoperiod, to adapt to current conditions and to prepare for environmental changes in the season to come. To assess photoperiodic responses at the protein level, we quantified the proteome of the model plant Arabidopsis thaliana by mass spectrometry across four photoperiods. This revealed coordinated changes of abundance in proteins of photosynthesis, primary and secondary metabolism, including pigment biosynthesis, consistent with higher metabolic activity in long photoperiods. Higher translation rates in the day than the night likely contribute to these changes, via an interaction with rhythmic changes in RNA abundance. Photoperiodic control of protein levels might be greatest only if high translation rates coincide with high transcript levels in some photoperiods. We term this proposed mechanism “translational coincidence”, mathematically model its components, and demonstrate its effect on the Arabidopsis proteome. Datasets from a green alga and a cyanobacterium suggest that translational coincidence contributes to seasonal control of the proteome in many phototrophic organisms. This may explain why many transcripts but not their cognate proteins exhibit diurnal rhythms.

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The Arabidopsis proteome changes in a coordinated fashion across four photoperiods. A simple ‘translational coincidence’ mechanism can explain photoperiod‐dependent regulation of protein levels based on clock‐dependent, daily mRNA level changes.

  • Day length altered the abundance of 1,781 proteins, out of 4,344 proteins quantified from leaves of Arabidopsis thaliana, in a pattern consistent with higher metabolic activity in long days.

  • Proteins with clock‐regulated, evening‐peaking RNAs tended to increase in abundance under longer daylengths, whereas proteins with morning‐peaking RNAs did not.

  • A simple, “translational coincidence” model predicted the experimental results, because high, light‐induced translation rates will coincide with high levels of an evening‐expressed RNA only under long days, not short days.

  • Many clock‐controlled genes might gain seasonal control of protein levels via translational coincidence, which we speculate is widespread based upon data from a marine alga and a freshwater cyanobacterium.

  • circadian rhythms
  • metabolism
  • photoperiod
  • proteomics
  • seasonality

Mol Syst Biol. (2018) 14: e7962

  • Received August 29, 2017.
  • Revision received January 22, 2018.
  • Accepted January 30, 2018.
  • © 2018 The Authors. Published under the terms of the CC BY 4.0 license

This is an open access article under the terms of the Creative Commons Attribution 4.0 License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Volume 14, Issue 3
01 March 2018
Molecular Systems Biology: 14 (3)
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