Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors

Abstract

Reactive oxygen species (ROS)-dependent signaling pathways from chloroplasts and mitochondria merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). RCD1 interacts in vivo and suppresses the activity of the transcription factors ANAC013 and ANAC017, which mediate a ROS-related retrograde signal originating from mitochondrial complex III. Inactivation of RCD1 leads to increased expression of mitochondrial dysfunction stimulon (MDS) genes regulated by ANAC013 and ANAC017. Accumulating MDS gene products, including alternative oxidases (AOXs), affect redox status of the chloroplasts, leading to changes in chloroplast ROS processing and increased protection of photosynthetic apparatus. ROS alter the abundance, thiol redox state and oligomerization of the RCD1 protein in vivo, providing feedback control on its function. RCD1-dependent regulation is linked to chloroplast signaling by 3'-phosphoadenosine 5'-phosphate (PAP). Thus, RCD1 integrates organellar signaling from chloroplasts and mitochondria to establish transcriptional control over the metabolic processes in both organelles.

Data availability

The atomic coordinates and structural restraints for the C-terminal domain of RCD1 have been deposited in the Protein Data Bank with the accession code 5N9Q.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Alexey Shapiguzov

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7199-1882
  2. Julia P Vainonen

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  3. Kerri Hunter

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2285-6999
  4. Helena Tossavainen

    Program in Structural Biology and Biophysics, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  5. Arjun Tiwari

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  6. Sari Järvi

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  7. Maarit Hellman

    Department of Chemistry, Nanoscience Center, University of Jyväskylä, Jyväskylä, Finland
    Competing interests
    The authors declare that no competing interests exist.
  8. Fayezeh Aarabi

    Max-Planck Institute for Molecular Plant Physiology, Potsdam-Golm, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Saleh Alseekh

    Max-Planck Institute for Molecular Plant Physiology, Potsdam-Golm, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2067-5235
  10. Brecht Wybouw

    Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8783-4646
  11. Katrien Van Der Kelen

    Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  12. Lauri Nikkanen

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  13. Julia Krasensky-Wrzaczek

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5989-9984
  14. Nina Sipari

    Viikki Metabolomics Unit, Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  15. Markku Keinänen

    Department of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, Finland
    Competing interests
    The authors declare that no competing interests exist.
  16. Esa Tyystjärvi

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  17. Eevi Rintamäki

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  18. Bert De Rybel

    Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9551-042X
  19. Jarkko Salojärvi

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4096-6278
  20. Frank van Breusegem

    Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  21. Alisdair R Fernie

    Max-Planck Institute for Molecular Plant Physiology, Potsdam-Golm, Germany
    Competing interests
    The authors declare that no competing interests exist.
  22. Mikael Brosché

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  23. Perttu Permi

    Program in Structural Biology and Biophysics, Institute of Biotechnology, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
  24. Eva-Mari Aro

    Department of Biochemistry / Molecular Plant Biology, University of Turku, Turku, Finland
    Competing interests
    The authors declare that no competing interests exist.
  25. Michael Wrzaczek

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5946-9060
  26. Jaakko Kangasjarvi

    Organismal and Evolutionary Biology Research Programme, Faculty of Biological and Environmental Sciences, and Viikki Plant Science Center, University of Helsinki, Helsinki, Finland
    For correspondence
    Jaakko.Kangasjarvi@helsinki.fi
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8959-1809

Funding

Helsingin Yliopisto

  • Jaakko Kangasjarvi

Suomen Akatemia

  • Jarkko Salojärvi
  • Eva-Mari Aro
  • Michael Wrzaczek
  • Jaakko Kangasjarvi

Fonds Wetenschappelijk Onderzoek

  • Brecht Wybouw
  • Bert De Rybel
  • Frank van Breusegem

Deutsche Forschungsgemeinschaft

  • Fayezeh Aarabi
  • Alisdair R Fernie

Horizon 2020 Framework Programme

  • Saleh Alseekh
  • Alisdair R Fernie

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

Reviewing Editor

  1. Christian S Hardtke, University of Lausanne, Switzerland

Version history

  1. Received: November 8, 2018
  2. Accepted: February 14, 2019
  3. Accepted Manuscript published: February 15, 2019 (version 1)
  4. Version of Record published: March 12, 2019 (version 2)

Copyright

© 2019, Shapiguzov 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. Alexey Shapiguzov
  2. Julia P Vainonen
  3. Kerri Hunter
  4. Helena Tossavainen
  5. Arjun Tiwari
  6. Sari Järvi
  7. Maarit Hellman
  8. Fayezeh Aarabi
  9. Saleh Alseekh
  10. Brecht Wybouw
  11. Katrien Van Der Kelen
  12. Lauri Nikkanen
  13. Julia Krasensky-Wrzaczek
  14. Nina Sipari
  15. Markku Keinänen
  16. Esa Tyystjärvi
  17. Eevi Rintamäki
  18. Bert De Rybel
  19. Jarkko Salojärvi
  20. Frank van Breusegem
  21. Alisdair R Fernie
  22. Mikael Brosché
  23. Perttu Permi
  24. Eva-Mari Aro
  25. Michael Wrzaczek
  26. Jaakko Kangasjarvi
(2019)
Arabidopsis RCD1 coordinates chloroplast and mitochondrial functions through interaction with ANAC transcription factors
eLife 8:e43284.
https://doi.org/10.7554/eLife.43284

Share this article

https://doi.org/10.7554/eLife.43284

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