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Title: 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.

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [3];  [4];  [3];  [5]; ORCiD logo [6]; ORCiD logo [7]
  1. MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States, Department of Plant Biology, Michigan State University, East Lansing, United States
  2. Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States
  3. Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
  4. MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
  5. Department of Plant Biology, Michigan State University, East Lansing, United States
  6. Department of Plant Biology, Michigan State University, East Lansing, United States, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
  7. MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States, Department of Plant Biology, Michigan State University, East Lansing, United States, Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, United States
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States); Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institute of Food and Agriculture
OSTI Identifier:
1577388
Alternate Identifier(s):
OSTI ID: 1577389; OSTI ID: 1628912; OSTI ID: 1735518
Grant/Contract Number:  
FG02-91ER20021; SC0018409; MCB1727362; MICL02598; NPGI-1811055
Resource Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 8; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Life Sciences & Biomedicine; Other Topics

Citation Formats

Cao, Pengfei, Kim, Sang-Jin, Xing, Anqi, Schenck, Craig A., Liu, Lu, Jiang, Nan, Wang, Jie, Last, Robert L., and Brandizzi, Federica. Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis. United States: N. p., 2019. Web. doi:10.7554/eLife.50747.
Cao, Pengfei, Kim, Sang-Jin, Xing, Anqi, Schenck, Craig A., Liu, Lu, Jiang, Nan, Wang, Jie, Last, Robert L., & Brandizzi, Federica. Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis. United States. https://doi.org/10.7554/eLife.50747
Cao, Pengfei, Kim, Sang-Jin, Xing, Anqi, Schenck, Craig A., Liu, Lu, Jiang, Nan, Wang, Jie, Last, Robert L., and Brandizzi, Federica. Fri . "Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis". United States. https://doi.org/10.7554/eLife.50747.
@article{osti_1577388,
title = {Homeostasis of branched-chain amino acids is critical for the activity of TOR signaling in Arabidopsis},
author = {Cao, Pengfei and Kim, Sang-Jin and Xing, Anqi and Schenck, Craig A. and Liu, Lu and Jiang, Nan and Wang, Jie and Last, Robert L. and Brandizzi, Federica},
abstractNote = {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.},
doi = {10.7554/eLife.50747},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {Fri Dec 06 00:00:00 EST 2019},
month = {Fri Dec 06 00:00:00 EST 2019}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.7554/eLife.50747

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Cited by: 49 works
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