1. Plant Biology

The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism

  1. Mohamad-Javad Vaseghi
  2. Kamel Chibani
  3. Wilena Telman
  4. Michael Florian Liebthal
  5. Melanie Gerken
  6. Helena Schnitzer
  7. Sara Mareike Mueller
  8. Karl-Josef Dietz  Is a corresponding author
  1. University of Bielefeld, Germany
https://doi.org/10.7554/eLife.38194
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Cite this article
  1. Mohamad-Javad Vaseghi
  2. Kamel Chibani
  3. Wilena Telman
  4. Michael Florian Liebthal
  5. Melanie Gerken
  6. Helena Schnitzer
  7. Sara Mareike Mueller
  8. Karl-Josef Dietz
(2018)
The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism
eLife 7:e38194.
https://doi.org/10.7554/eLife.38194
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Abstract

Thiol-dependent redox regulation controls central processes in plant cells including photosynthesis. Thioredoxins reductively activate e.g. Calvin-Benson cycle enzymes. However the mechanism of oxidative inactivation is unknown despite its importance for efficient regulation. Here, the abundant 2-cysteine peroxiredoxin (2-CysPrx), but not its site-directed variants, mediates rapid inactivation of reductively activated fructose-1,6-bisphosphatase and NADPH-dependent malate dehydrogenase (MDH) in the presence of the proper thioredoxins. Deactivation of phosphoribulokinase (PRK) and MDH was compromised in 2cysprxAB mutant plants upon light/dark transition compared to wildtype. The decisive role of 2-CysPrx in regulating photosynthesis was evident from reoxidation kinetics of ferredoxin upon darkening of intact leaves since its half time decreased 3.5-times in 2cysprxAB. The disadvantage of inefficient deactivation turned into an advantage in fluctuating light. Physiological parameters like MDH and PRK inactivation, photosynthetic kinetics and response to fluctuating light fully recovered in 2cysprxAB mutants complemented with 2-CysPrxA underlining the significance of 2-CysPrx. The results show that the 2-CysPrx serves as electron sink in the thiol network important to oxidize reductively activated proteins and represents the missing link in the reversal of thioredoxin-dependent regulation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Original and aggregated data are provided in the supplementary data file.

Article and author information

Author details

  1. Mohamad-Javad Vaseghi

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Kamel Chibani

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Wilena Telman

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  4. Michael Florian Liebthal

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  5. Melanie Gerken

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  6. Helena Schnitzer

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1027-1803

  7. Sara Mareike Mueller

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

  8. Karl-Josef Dietz

    Department of Biochemistry and Physiology of Plants, Faculty of Biology, University of Bielefeld, Bielefeld, Germany
    For correspondence
    karl-josef.dietz@uni-bielefeld.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0311-2182

Funding

Deutsche Forschungsgemeinschaft (Di346/14)

  • Karl-Josef Dietz

Deutsche Forschungsgemeinschaft (SPP1710)

  • Karl-Josef Dietz

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

Reviewing Editor

  1. Christine Foyer, University of Leeds, United Kingdom

Version history

  1. Received: May 8, 2018
  2. Accepted: October 7, 2018
  3. Accepted Manuscript published: October 12, 2018 (version 1)
  4. Version of Record published: November 7, 2018 (version 2)
  5. Version of Record updated: November 9, 2018 (version 3)

Copyright

© 2018, Vaseghi 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. Mohamad-Javad Vaseghi
  2. Kamel Chibani
  3. Wilena Telman
  4. Michael Florian Liebthal
  5. Melanie Gerken
  6. Helena Schnitzer
  7. Sara Mareike Mueller
  8. Karl-Josef Dietz
(2018)
The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism
eLife 7:e38194.
https://doi.org/10.7554/eLife.38194

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