1. Plant Biology
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The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism

Research Article
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Cite this article as: eLife 2018;7:e38194 doi: 10.7554/eLife.38194

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

Publication 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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Further reading

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    Stem cell homeostasis in plant shoot meristems requires tight coordination between stem cell proliferation and cell differentiation. In Arabidopsis, stem cells express the secreted dodecapeptide CLAVATA3 (CLV3), which signals through the leucine-rich repeat (LRR)-receptor kinase CLAVATA1 (CLV1) and related CLV1-family members to downregulate expression of the homeodomain transcription factor WUSCHEL (WUS). WUS protein moves from cells below the stem cell domain to the meristem tip and promotes stem cell identity, together with CLV3 expression, generating a negative feedback loop. How stem cell activity in the meristem centre is coordinated with organ initiation and cell differentiation at the periphery is unknown. We show here that the CLE40 gene, encoding a secreted peptide closely related to CLV3, is expressed in the SAM in differentiating cells in a pattern complementary to that of CLV3. CLE40 promotes WUS expression via BAM1, a CLV1-family receptor, and CLE40 expression is in turn repressed in a WUS-dependent manner. Together, CLE40-BAM1-WUS establish a second negative feedback loop. We propose that stem cell homeostasis is achieved through two intertwined pathways that adjust WUS activity and incorporate information on the size of the stem cell domain, via CLV3-CLV1, and on cell differentiation via CLE40-BAM1.