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Research ArticleBREAKTHROUGH REPORTS
Open Access

Synergism between Inositol Polyphosphates and TOR Kinase Signaling in Nutrient Sensing, Growth Control, and Lipid Metabolism in Chlamydomonas

Inmaculada Couso, Bradley S. Evans, Jia Li, Yu Liu, Fangfang Ma, Spencer Diamond, Doug K. Allen, James G. Umen
Inmaculada Couso
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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Bradley S. Evans
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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Jia Li
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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Yu Liu
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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Fangfang Ma
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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Spencer Diamond
bEarth and Planetary Science, University of California, Berkeley, California 94720
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Doug K. Allen
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
cAgricultural Research Service, U.S. Department of Agriculture, St. Louis, Missouri 63132
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James G. Umen
aDonald Danforth Plant Science Center, St. Louis, Missouri 63132
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  • For correspondence: jumen@danforthcenter.org

Published September 2016. DOI: https://doi.org/10.1105/tpc.16.00351

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  • © 2016 American Society of Plant Biologists. All rights reserved.

Abstract

The networks that govern carbon metabolism and control intracellular carbon partitioning in photosynthetic cells are poorly understood. Target of Rapamycin (TOR) kinase is a conserved growth regulator that integrates nutrient signals and modulates cell growth in eukaryotes, though the TOR signaling pathway in plants and algae has yet to be completely elucidated. We screened the unicellular green alga Chlamydomonas reinhardtii using insertional mutagenesis to find mutants that conferred hypersensitivity to the TOR inhibitor rapamycin. We characterized one mutant, vip1-1, that is predicted to encode a conserved inositol hexakisphosphate kinase from the VIP family that pyrophosphorylates phytic acid (InsP6) to produce the low abundance signaling molecules InsP7 and InsP8. Unexpectedly, the rapamycin hypersensitive growth arrest of vip1-1 cells was dependent on the presence of external acetate, which normally has a growth-stimulatory effect on Chlamydomonas. vip1-1 mutants also constitutively overaccumulated triacylglycerols (TAGs) in a manner that was synergistic with other TAG inducing stimuli such as starvation. vip1-1 cells had reduced InsP7 and InsP8, both of which are dynamically modulated in wild-type cells by TOR kinase activity and the presence of acetate. Our data uncover an interaction between the TOR kinase and inositol polyphosphate signaling systems that we propose governs carbon metabolism and intracellular pathways that lead to storage lipid accumulation.

  • Glossary

    rapHS
    rapamycin hypersensitive
    LC-MS/MS
    liquid chromatography and tandem mass spectrometry
    TLC
    thin-layer chromatography
    TAG
    triacylglycerol
    TCA
    tricarboxylic acid
    FW
    fresh weight
    FAME
    fatty acid methyl ester
    GC-FID
    gas chromatography-flame ionization detection
    DIC
    differential interference contrast
    • Received May 3, 2016.
    • Revised August 19, 2016.
    • Accepted September 2, 2016.
    • Published September 6, 2016.

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    Synergism between Inositol Polyphosphates and TOR Kinase Signaling in Nutrient Sensing, Growth Control, and Lipid Metabolism in Chlamydomonas
    Inmaculada Couso, Bradley S. Evans, Jia Li, Yu Liu, Fangfang Ma, Spencer Diamond, Doug K. Allen, James G. Umen
    The Plant Cell Sep 2016, 28 (9) 2026-2042; DOI: 10.1105/tpc.16.00351

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    Synergism between Inositol Polyphosphates and TOR Kinase Signaling in Nutrient Sensing, Growth Control, and Lipid Metabolism in Chlamydomonas
    Inmaculada Couso, Bradley S. Evans, Jia Li, Yu Liu, Fangfang Ma, Spencer Diamond, Doug K. Allen, James G. Umen
    The Plant Cell Sep 2016, 28 (9) 2026-2042; DOI: 10.1105/tpc.16.00351
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    The Plant Cell: 28 (9)
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    Sep 2016
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