LPCAT1 controls phosphate homeostasis in a zinc-dependent manner

  1. Mushtak Kisko
  2. Nadia Bouain
  3. Alaeddine Safi
  4. Anna Medici
  5. Robert C Akkers
  6. David Secco
  7. Gilles Fouret
  8. Gabriel Krouk
  9. Mark GM Aarts
  10. Wolfgang Busch
  11. Hatem Rouached  Is a corresponding author
  1. INRA, France
  2. Wageningen University, Netherlands
  3. CNRS, France
  4. Salk Institute for Biological Studies, United States

Abstract

All living organisms require a variety of essential elements for their basic biological functions. While the homeostasis of nutrients is highly intertwined, the molecular and genetic mechanisms of these dependencies remains poorly understood. Here, we report a discovery of a molecular pathway that control phosphate (Pi) accumulation plants in Zn deficiency. Using genome-wide association studies we first identified allelic variation of the Lyso-PhosphatidylCholine (PC) AcylTransferase 1 (LPCAT1) gene as the key determinant of shoot Pi accumulation under Zn deficiency. We then show that regulatory variation at the LPCAT1 locus contributes significantly to this natural variation and we further demonstrate that the regulation of LPCAT1 expression involves bZIP23 TF, for which we identified a new binding site sequence. Finally, we show that in Zn deficient conditions loss of function of LPCAT1 increases the phospholipid Lyso-PhosphatidylCholine/PhosphatidylCholine ratio, the expression of the Pi transporter PHT1;1, and that this leads to shoot Pi accumulation.

Article and author information

Author details

  1. Mushtak Kisko

    Biochimie et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Nadia Bouain

    Biochimie et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Alaeddine Safi

    Biochime et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1532-5708
  4. Anna Medici

    Biochimie et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Robert C Akkers

    Laboratory of Genetics, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. David Secco

    Biochimie et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Gilles Fouret

    Unité Mixte de Recherche 866, INRA, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Gabriel Krouk

    INSB, CNRS, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Mark GM Aarts

    Laboratory of Genetics, Wageningen University, Wageningen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Wolfgang Busch

    Plant Molecular and Cellular Biology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Hatem Rouached

    Biochimie et Physiologie Moléculaire des Plantes, INRA, Montpellier, France
    For correspondence
    hatem.rouached@supagro.inra.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7751-0477

Funding

Institut National de la Recherche Agronomique

  • Hatem Rouached

The Austrian Academy of Sciences through Gregor Mendel Institute

  • Wolfgang Busch

The Netherland Genome Initiative ZonMW Horizon program Zenith (no. 40-41009-98-11084)

  • Mark GM Aarts

Iraq Government Doctoral Fellowship

  • Mushtak Kisko

Région Languedoc-Roussillon: Chercheurd'Avenir/Projet Cofinancé par le Fonds Européen de Développement Regional

  • Hatem Rouached

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

Copyright

© 2018, Kisko 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

  • 3,018
    views
  • 496
    downloads
  • 64
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Mushtak Kisko
  2. Nadia Bouain
  3. Alaeddine Safi
  4. Anna Medici
  5. Robert C Akkers
  6. David Secco
  7. Gilles Fouret
  8. Gabriel Krouk
  9. Mark GM Aarts
  10. Wolfgang Busch
  11. Hatem Rouached
(2018)
LPCAT1 controls phosphate homeostasis in a zinc-dependent manner
eLife 7:e32077.
https://doi.org/10.7554/eLife.32077

Share this article

https://doi.org/10.7554/eLife.32077

Further reading

    1. Microbiology and Infectious Disease
    2. Plant Biology
    Nyasha Charura, Ernesto Llamas ... Alga Zuccaro
    Research Article

    Programmed cell death occurring during plant development (dPCD) is a fundamental process integral for plant growth and reproduction. Here, we investigate the connection between developmentally controlled PCD and fungal accommodation in Arabidopsis thaliana roots, focusing on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB) and the senescence-associated nuclease BFN1. Mutations of both dPCD regulators increase colonization by the beneficial fungus Serendipita indica, primarily in the differentiation zone. smb-3 mutants additionally exhibit hypercolonization around the meristematic zone and a delay of S. indica-induced root-growth promotion. This demonstrates that root cap dPCD and rapid post-mortem clearance of cellular corpses represent a physical defense mechanism restricting microbial invasion of the root. Additionally, reporter lines and transcriptional analysis revealed that BFN1 expression is downregulated during S. indica colonization in mature root epidermal cells, suggesting a transcriptional control mechanism that facilitates the accommodation of beneficial microbes in the roots.

    1. Cell Biology
    2. Plant Biology
    Masanori Izumi, Sakuya Nakamura ... Shinya Hagihara
    Research Article

    Plants distribute many nutrients to chloroplasts during leaf development and maturation. When leaves senesce or experience sugar starvation, the autophagy machinery degrades chloroplast proteins to facilitate efficient nutrient reuse. Here, we report on the intracellular dynamics of an autophagy pathway responsible for piecemeal degradation of chloroplast components. Through live-cell monitoring of chloroplast morphology, we observed the formation of chloroplast budding structures in sugar-starved leaves. These buds were then released and incorporated into the vacuolar lumen as an autophagic cargo termed a Rubisco-containing body. The budding structures did not accumulate in mutants of core autophagy machinery, suggesting that autophagosome creation is required for forming chloroplast buds. Simultaneous tracking of chloroplast morphology and autophagosome development revealed that the isolation membranes of autophagosomes interact closely with part of the chloroplast surface before forming chloroplast buds. Chloroplasts then protrude at the site associated with the isolation membranes, which divide synchronously with autophagosome maturation. This autophagy-related division does not require DYNAMIN-RELATED PROTEIN 5B, which constitutes the division ring for chloroplast proliferation in growing leaves. An unidentified division machinery may thus fragment chloroplasts for degradation in coordination with the development of the chloroplast-associated isolation membrane.