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.

Metrics

  • 2,756
    Page views
  • 424
    Downloads
  • 12
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Plant Biology
    Asako Ishii, Jianyu Shan ... Jun Minagawa
    Research Article

    As a ubiquitous picophytoplankton in the ocean and an early-branching green alga, Ostreococcus tauri is a model prasinophyte species for studying the functional evolution of the light-harvesting systems in photosynthesis. Here, we report the structure and function of the O. tauri photosystem I (PSI) supercomplex in low light conditions, where it expands its photon-absorbing capacity by assembling with the light-harvesting complexes I (LHCI) and a prasinophyte-specific light-harvesting complex (Lhcp). The architecture of the supercomplex exhibits hybrid features of the plant-type and the green algal-type PSI supercomplexes, consisting of a PSI core, a Lhca1-Lhca4-Lhca2-Lhca3 belt attached on one side and a Lhca5-Lhca6 heterodimer associated on the other side between PsaG and PsaH. Interestingly, nine Lhcp subunits, including one Lhcp1 monomer with a phosphorylated amino-terminal threonine and eight Lhcp2 monomers, oligomerize into three trimers and associate with PSI on the third side between Lhca6 and PsaK. The Lhcp1 phosphorylation and the light-harvesting capacity of PSI were subjected to reversible photoacclimation, suggesting that the formation of OtPSI-LHCI-Lhcp supercomplex is likely due to a phosphorylation-dependent mechanism induced by changes in light intensity. Notably, this supercomplex did not exhibit far-red peaks in the 77 K fluorescence spectra, which is possibly due to the weak coupling of the chlorophyll a603-a609 pair in OtLhca1-4.

    1. Chromosomes and Gene Expression
    2. Plant Biology
    Vy Nguyen, Iain Searle
    Insight

    A well-established model for how plants start the process of flowering in periods of cold weather may need revisiting.