Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis

Abstract

The target of rapamycin (TOR) kinase is an evolutionarily conserved hub of nutrient sensing and metabolic signaling. In plants, a functional connection of TOR activation with glucose availability was demonstrated, while it is yet unclear whether branched-chain amino acids (BCAAs) are a primary input of TOR signaling as they are in yeast and mammalian cells. Here, we report on the characterization of an Arabidopsis mutant over-accumulating BCAAs. Through chemical interventions targeting TOR and by examining mutants of BCAA biosynthesis and TOR signaling, we found that BCAA over-accumulation leads to up-regulation of TOR activity, which causes reorganization of the actin cytoskeleton and actin-associated endomembranes. Finally, we show that activation of TOR is concomitant with alteration of cell expansion, proliferation and specialized metabolism, leading to pleiotropic effects on plant growth and development. These results demonstrate that BCAAs contribute to plant TOR activation and reveal previously uncharted downstream subcellular processes of TOR signaling.

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All data generated or analyzed in this study have been included in the manuscript and the supporting files.

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Author details

  1. Pengfei Cao

    MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6998-9302
  2. Sang-Jin Kim

    Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Anqi Xing

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Craig A Schenck

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5711-7213
  5. Lu Liu

    MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Nan Jiang

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jie Wang

    Department of Plant Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Robert L Last

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6974-9587
  9. Federica Brandizzi

    MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
    For correspondence
    fb@msu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0580-8888

Funding

National Science Foundation (MCB1727362)

  • Federica Brandizzi

National Institute of Food and Agriculture (MICL02299)

  • Federica Brandizzi

National Science Foundation (NPGI-1811055)

  • Craig A Schenck

U.S. Department of Energy (DE-FG02-91ER20021)

  • Federica Brandizzi

U.S. Department of Energy (DE-FC02-07ER64494)

  • Federica Brandizzi

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

Version history

  1. Received: August 1, 2019
  2. Accepted: December 5, 2019
  3. Accepted Manuscript published: December 6, 2019 (version 1)
  4. Version of Record published: December 30, 2019 (version 2)

Copyright

© 2019, Cao 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. Pengfei Cao
  2. Sang-Jin Kim
  3. Anqi Xing
  4. Craig A Schenck
  5. Lu Liu
  6. Nan Jiang
  7. Jie Wang
  8. Robert L Last
  9. Federica Brandizzi
(2019)
Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis
eLife 8:e50747.
https://doi.org/10.7554/eLife.50747

Share this article

https://doi.org/10.7554/eLife.50747

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