Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis

  1. Jinsheng Zhu
  2. Kelvin Lau
  3. Robert Puschmann
  4. Robert K Harmel
  5. Youjun Zhang
  6. Verena Pries
  7. Philipp Gaugler
  8. Larissa Broger
  9. Amit K Dutta
  10. Henning J Jessen
  11. Gabriel Schaaf
  12. Alisdair R Fernie
  13. Ludwig A Hothorn
  14. Dorothea Fiedler
  15. Michael Hothorn  Is a corresponding author
  1. University of Geneva, Switzerland
  2. Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Germany
  3. Max-Planck Institute of Molecular Plant Physiology, Germany
  4. University of Bonn, Germany
  5. Albert-Ludwigs-Universität Freiburg, Germany
  6. Max-Planck Institute for Molecular Plant Physiology, Germany
  7. Leibniz University, Germany

Abstract

Many eukaryotic proteins regulating phosphate (Pi) homeostasis contain SPX domains that are receptors for inositol pyrophosphates (PP-InsP), suggesting that PP-InsPs may regulate Pi homeostasis. Here we report that deletion of two diphosphoinositol pentakisphosphate kinases VIH1/2 impairs plant growth and leads to constitutive Pi starvation responses. Deletion of phosphate starvation response transcription factors partially rescues vih1 vih2 mutant phenotypes, placing diphosphoinositol pentakisphosphate kinases in plant Pi signal transduction cascades. VIH1/2 are bifunctional enzymes able to generate and break-down PP-InsPs. Mutations in the kinase active site lead to increased Pi levels and constitutive Pi starvation responses. ATP levels change significantly in different Pi growth conditions. ATP-Mg2+ concentrations shift the relative kinase and phosphatase activities of diphosphoinositol pentakisphosphate kinases in vitro. Pi inhibits the phosphatase activity of the enzyme. Thus, VIH1 and VIH2 relay changes in cellular ATP and Pi concentrations to changes in PP-InsP levels, allowing plants to maintain sufficient Pi levels.

Data availability

Pi measurements: raw data included in actual figurePhenotypes: representative lines shown in main figures, at least three independent lines shown in figure supplementsWestern blots: full western blots shown in figure supplementsProtein gels: Full gels shown in figure 5 supplement 1 and figure 6 supplement 1DNA sequences of the truncated VIH2 transcript is in figure 2 supplement 1NMR data: full 1D and 2D spectra shown in figure 5 and figure 5 supplement 2, figure 6 supplement 2

Article and author information

Author details

  1. Jinsheng Zhu

    Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneve, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8131-1876
  2. Kelvin Lau

    Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneve, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert Puschmann

    Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6443-2326
  4. Robert K Harmel

    Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Youjun Zhang

    Max-Planck Institute of Molecular Plant Physiology, Potsdam-Golm, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Verena Pries

    Department of Plant Nutrition, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Philipp Gaugler

    Department of Plant Nutrition, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Larissa Broger

    Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneve, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  9. Amit K Dutta

    Institute of Organic Chemistry, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Henning J Jessen

    Institute of Organic Chemistry, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Gabriel Schaaf

    Institute of Crop Science and Resource Conservation, Department of Plant Nutrition, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Alisdair R Fernie

    Max-Planck Institute for Molecular Plant Physiology, Potsdam-Golm, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Ludwig A Hothorn

    Institute of Biostatistics, Leibniz University, Hannover, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Dorothea Fiedler

    Leibniz-Forschungsinstitut für Molekulare Pharmakologie, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Michael Hothorn

    Structural Plant Biology Laboratory, Department of Botany and Plant Biology, University of Geneva, Geneve, Switzerland
    For correspondence
    michael.hothorn@unige.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3597-5698

Funding

H2020 European Research Council (310856)

  • Michael Hothorn

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (CRSII5_170925)

  • Dorothea Fiedler
  • Michael Hothorn

Howard Hughes Medical Institute (55008733)

  • Michael Hothorn

European Molecular Biology Organization (ALTF 493-2015)

  • Kelvin Lau

Leibniz-Gemeinschaft (SAW-2017-FMP-1)

  • Dorothea Fiedler

Deutsche Forschungsgemeinschaft (SCHA 1274/4-1)

  • Gabriel Schaaf

Max-Planck-Gesellschaft

  • Youjun Zhang
  • Alisdair R Fernie

Horizon 2020 Framework Programme (PlantaSYST)

  • Youjun Zhang
  • 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. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Publication history

  1. Received: November 12, 2018
  2. Accepted: August 21, 2019
  3. Accepted Manuscript published: August 22, 2019 (version 1)
  4. Version of Record published: September 6, 2019 (version 2)

Copyright

© 2019, Zhu 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. Jinsheng Zhu
  2. Kelvin Lau
  3. Robert Puschmann
  4. Robert K Harmel
  5. Youjun Zhang
  6. Verena Pries
  7. Philipp Gaugler
  8. Larissa Broger
  9. Amit K Dutta
  10. Henning J Jessen
  11. Gabriel Schaaf
  12. Alisdair R Fernie
  13. Ludwig A Hothorn
  14. Dorothea Fiedler
  15. Michael Hothorn
(2019)
Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis
eLife 8:e43582.
https://doi.org/10.7554/eLife.43582

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