SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants

  1. Andrea Mair
  2. Lorenzo Pedrotti
  3. Bernhard Wurzinger
  4. Dorothea Anrather
  5. Andrea Simeunovic
  6. Christoph Weiste
  7. Concetta Valerio
  8. Katrin Dietrich
  9. Tobias Kirchler
  10. Thomas Nägele
  11. Jesús Vicente Carbajosa
  12. Johannes Hanson
  13. Elena Baena-González
  14. Christina Chaban
  15. Wolfram Weckwerth
  16. Wolfgang Dröge-Laser
  17. Markus Teige  Is a corresponding author
  1. University of Vienna, Austria
  2. University of Würzburg, Germany
  3. Instituto Gulbenkian de Ciência, Portugal
  4. University of Tübingen, Germany
  5. Universidad Politécnica de Madrid, Spain
  6. Utrecht University, Netherlands

Abstract

Metabolic adjustment to changing environmental conditions, particularly balancing of growth and defense responses, is crucial for all organisms to survive. The evolutionary conserved AMPK/Snf1/SnRK1 kinases are well-known metabolic master regulators in the low-energy response in animals, yeast and plants. They act at two different levels: by modulating the activity of key metabolic enzymes, and by massive transcriptional reprogramming. While the first part is well established, the latter function is only partially understood in animals and not at all in plants. Here we identified the Arabidopsis transcription factor bZIP63 as key regulator of the starvation response and direct target of the SnRK1 kinase. Phosphorylation of bZIP63 by SnRK1 changed its dimerization preference, thereby affecting target gene expression and ultimately primary metabolism. A bzip63 knock-out mutant exhibited starvation-related phenotypes, which could be functionally complemented by wild type bZIP63, but not by a version harboring point mutations in the identified SnRK1 target sites.

Article and author information

Author details

  1. Andrea Mair

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  2. Lorenzo Pedrotti

    Pharmaceutical Biology, Julius-von-Sachs-Institute, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Bernhard Wurzinger

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  4. Dorothea Anrather

    University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Andrea Simeunovic

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  6. Christoph Weiste

    Pharmaceutical Biology, Julius-von-Sachs-Institute, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Concetta Valerio

    Instituto Gulbenkian de Ciência, Oeiras, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  8. Katrin Dietrich

    Pharmaceutical Biology, Julius-von-Sachs-Institute, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Tobias Kirchler

    Department of Plant Physiology, Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Thomas Nägele

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  11. Jesús Vicente Carbajosa

    Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  12. Johannes Hanson

    Department of Molecular Plant Physiology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Elena Baena-González

    Instituto Gulbenkian de Ciência, Oeiras, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  14. Christina Chaban

    Department of Plant Physiology, Center for Plant Molecular Biology, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Wolfram Weckwerth

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  16. Wolfgang Dröge-Laser

    Pharmaceutical Biology, Julius-von-Sachs-Institute, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Markus Teige

    Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria
    For correspondence
    markus.teige@univie.ac.at
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Thorsten Nürnberger, University of Tubingen, Germany

Version history

  1. Received: November 30, 2014
  2. Accepted: August 10, 2015
  3. Accepted Manuscript published: August 11, 2015 (version 1)
  4. Accepted Manuscript updated: August 18, 2015 (version 2)
  5. Version of Record published: September 3, 2015 (version 3)

Copyright

© 2015, Mair 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

  • 5,964
    Page views
  • 1,815
    Downloads
  • 175
    Citations

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

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. Andrea Mair
  2. Lorenzo Pedrotti
  3. Bernhard Wurzinger
  4. Dorothea Anrather
  5. Andrea Simeunovic
  6. Christoph Weiste
  7. Concetta Valerio
  8. Katrin Dietrich
  9. Tobias Kirchler
  10. Thomas Nägele
  11. Jesús Vicente Carbajosa
  12. Johannes Hanson
  13. Elena Baena-González
  14. Christina Chaban
  15. Wolfram Weckwerth
  16. Wolfgang Dröge-Laser
  17. Markus Teige
(2015)
SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants
eLife 4:e05828.
https://doi.org/10.7554/eLife.05828

Share this article

https://doi.org/10.7554/eLife.05828

Further reading

    1. Cell Biology
    2. Neuroscience
    Haibin Yu, Dandan Liu ... Kai Yuan
    Research Article

    O-GlcNAcylation is a dynamic post-translational modification that diversifies the proteome. Its dysregulation is associated with neurological disorders that impair cognitive function, and yet identification of phenotype-relevant candidate substrates in a brain-region specific manner remains unfeasible. By combining an O-GlcNAc binding activity derived from Clostridium perfringens OGA (CpOGA) with TurboID proximity labeling in Drosophila, we developed an O-GlcNAcylation profiling tool that translates O-GlcNAc modification into biotin conjugation for tissue-specific candidate substrates enrichment. We mapped the O-GlcNAc interactome in major brain regions of Drosophila and found that components of the translational machinery, particularly ribosomal subunits, were abundantly O-GlcNAcylated in the mushroom body of Drosophila brain. Hypo-O-GlcNAcylation induced by ectopic expression of active CpOGA in the mushroom body decreased local translational activity, leading to olfactory learning deficits that could be rescued by dMyc overexpression-induced increase of protein synthesis. Our study provides a useful tool for future dissection of tissue-specific functions of O-GlcNAcylation in Drosophila, and suggests a possibility that O-GlcNAcylation impacts cognitive function via regulating regional translational activity in the brain.

    1. Cancer Biology
    2. Cell Biology
    Ibtisam Ibtisam, Alexei F Kisselev
    Short Report

    Rapid recovery of proteasome activity may contribute to intrinsic and acquired resistance to FDA-approved proteasome inhibitors. Previous studies have demonstrated that the expression of proteasome genes in cells treated with sub-lethal concentrations of proteasome inhibitors is upregulated by the transcription factor Nrf1 (NFE2L1), which is activated by a DDI2 protease. Here, we demonstrate that the recovery of proteasome activity is DDI2-independent and occurs before transcription of proteasomal genes is upregulated but requires protein translation. Thus, mammalian cells possess an additional DDI2 and transcription-independent pathway for the rapid recovery of proteasome activity after proteasome inhibition.