Regulation of photosynthetic electron flow on dark to light transition by Ferredoxin:NADP(H) Oxidoreductase interactions

  1. Manuela Kramer
  2. Melvin Rodriguez-Heredia
  3. Francesco Saccon
  4. Laura Mosebach
  5. Manuel Twachtmann
  6. Anja Krieger-Liszkay
  7. Chris Duffy
  8. Robert J Knell
  9. Giovanni Finazzi
  10. Guy Thomas Hanke  Is a corresponding author
  1. Queen Mary University of London, United Kingdom
  2. University of Münster, Germany
  3. University of Osnabrueck, Germany
  4. CNRS, France
  5. CEA-Grenoble, France

Abstract

During photosynthesis, electron transport is necessary for carbon assimilation and must be regulated to minimize free radical damage. There is a longstanding controversy over the role of a critical enzyme in this process (ferredoxin:NADP(H) oxidoreductase, or FNR), and in particular its location within chloroplasts. Here we use immunogold labelling to prove that FNR previously assigned as soluble is in fact membrane associated. We combined this technique with a genetic approach in the model plant Arabidopsis, to show that the distribution of this enzyme between different membrane regions depends on its interaction with specific tether proteins. We further demonstrate a correlation between the interaction of FNR with different proteins and the activity of alternative photosynthetic electron transport pathways. This supports a role for FNR location in regulating photosynthetic electron flow during the transition from dark to light.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files, except individual electron micrographs. Micrographs of chloroplasts that were analysed have been deposited at Dryad (https://doi.org/10.5061/dryad.7d7wm37rs) for full transparency. These are marked, to indicate the areas of the chloroplast analysed.

Article and author information

Author details

  1. Manuela Kramer

    Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Melvin Rodriguez-Heredia

    Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Francesco Saccon

    School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura Mosebach

    Institute of Plant Biology and Biotechnology,, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Manuel Twachtmann

    Plant Physiology, University of Osnabrueck, Osnabrueck, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Anja Krieger-Liszkay

    4Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Saclay, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Chris Duffy

    Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Robert J Knell

    School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3446-8715
  9. Giovanni Finazzi

    CEA-Grenoble, Grenoble, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Guy Thomas Hanke

    Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
    For correspondence
    g.hanke@qmul.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6167-926X

Funding

Deutsche Forschungsgemeinschaft (SFB944 project 2)

  • Guy Thomas Hanke

Biotechnology and Biological Sciences Research Council (BB/R004838/1)

  • Guy Thomas Hanke

University Grenoble Alpes graduate school (ANR-10-LABX-49-01)

  • Giovanni Finazzi

European Research Council (ERC Chloro-mito (833184)

  • Giovanni Finazzi

LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS)

  • Anja Krieger-Liszkay

French Infrastructure for Integrated Structural Biology (ANR-10-INSB-05)

  • Anja Krieger-Liszkay

Bayer CropScience (F-2016-BS-0555)

  • Manuela Kramer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David M Kramer, Michigan State University, United States

Publication history

  1. Received: February 17, 2020
  2. Accepted: February 25, 2021
  3. Accepted Manuscript published: March 9, 2021 (version 1)
  4. Version of Record published: March 22, 2021 (version 2)

Copyright

© 2021, Kramer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Manuela Kramer
  2. Melvin Rodriguez-Heredia
  3. Francesco Saccon
  4. Laura Mosebach
  5. Manuel Twachtmann
  6. Anja Krieger-Liszkay
  7. Chris Duffy
  8. Robert J Knell
  9. Giovanni Finazzi
  10. Guy Thomas Hanke
(2021)
Regulation of photosynthetic electron flow on dark to light transition by Ferredoxin:NADP(H) Oxidoreductase interactions
eLife 10:e56088.
https://doi.org/10.7554/eLife.56088

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