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The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis

Energy is essential for all cellular functions in a living organism. How cells coordinate their physiological processes with energy status and availability is thus an important question. The turnover of actin cytoskeleton between its monomeric and filamentous forms is a major energy drain in eukaryo...

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Autores principales: Dai, Liufeng, Wang, Baojie, Wang, Ting, Meyer, Etienne H., Kettel, Valentin, Hoffmann, Natalie, McFarlane, Heather E., Li, Shalan, Wu, Xuna, Picard, Kelsey L., Giavalisco, Patrick, Persson, Staffan, Zhang, Yi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499549/
https://www.ncbi.nlm.nih.gov/pubmed/36095209
http://dx.doi.org/10.1073/pnas.2122969119
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author Dai, Liufeng
Wang, Baojie
Wang, Ting
Meyer, Etienne H.
Kettel, Valentin
Hoffmann, Natalie
McFarlane, Heather E.
Li, Shalan
Wu, Xuna
Picard, Kelsey L.
Giavalisco, Patrick
Persson, Staffan
Zhang, Yi
author_facet Dai, Liufeng
Wang, Baojie
Wang, Ting
Meyer, Etienne H.
Kettel, Valentin
Hoffmann, Natalie
McFarlane, Heather E.
Li, Shalan
Wu, Xuna
Picard, Kelsey L.
Giavalisco, Patrick
Persson, Staffan
Zhang, Yi
author_sort Dai, Liufeng
collection PubMed
description Energy is essential for all cellular functions in a living organism. How cells coordinate their physiological processes with energy status and availability is thus an important question. The turnover of actin cytoskeleton between its monomeric and filamentous forms is a major energy drain in eukaryotic cells. However, how actin dynamics are regulated by ATP levels remain largely unknown in plant cells. Here, we observed that seedlings with impaired functions of target of rapamycin complex 1 (TORC1), either by mutation of the key component, RAPTOR1B, or inhibition of TOR activity by specific inhibitors, displayed reduced sensitivity to actin cytoskeleton disruptors compared to their controls. Consistently, actin filament dynamics, but not organization, were suppressed in TORC1-impaired cells. Subcellular localization analysis and quantification of ATP concentration demonstrated that RAPTOR1B localized at cytoplasm and mitochondria and that ATP levels were significantly reduced in TORC1-impaired plants. Further pharmacologic experiments showed that the inhibition of mitochondrial functions led to phenotypes mimicking those observed in raptor1b mutants at the level of both plant growth and actin dynamics. Exogenous feeding of adenine could partially restore ATP levels and actin dynamics in TORC1-deficient plants. Thus, these data support an important role for TORC1 in coordinating ATP homeostasis and actin dynamics in plant cells.
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spelling pubmed-94995492022-09-23 The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis Dai, Liufeng Wang, Baojie Wang, Ting Meyer, Etienne H. Kettel, Valentin Hoffmann, Natalie McFarlane, Heather E. Li, Shalan Wu, Xuna Picard, Kelsey L. Giavalisco, Patrick Persson, Staffan Zhang, Yi Proc Natl Acad Sci U S A Biological Sciences Energy is essential for all cellular functions in a living organism. How cells coordinate their physiological processes with energy status and availability is thus an important question. The turnover of actin cytoskeleton between its monomeric and filamentous forms is a major energy drain in eukaryotic cells. However, how actin dynamics are regulated by ATP levels remain largely unknown in plant cells. Here, we observed that seedlings with impaired functions of target of rapamycin complex 1 (TORC1), either by mutation of the key component, RAPTOR1B, or inhibition of TOR activity by specific inhibitors, displayed reduced sensitivity to actin cytoskeleton disruptors compared to their controls. Consistently, actin filament dynamics, but not organization, were suppressed in TORC1-impaired cells. Subcellular localization analysis and quantification of ATP concentration demonstrated that RAPTOR1B localized at cytoplasm and mitochondria and that ATP levels were significantly reduced in TORC1-impaired plants. Further pharmacologic experiments showed that the inhibition of mitochondrial functions led to phenotypes mimicking those observed in raptor1b mutants at the level of both plant growth and actin dynamics. Exogenous feeding of adenine could partially restore ATP levels and actin dynamics in TORC1-deficient plants. Thus, these data support an important role for TORC1 in coordinating ATP homeostasis and actin dynamics in plant cells. National Academy of Sciences 2022-09-12 2022-09-20 /pmc/articles/PMC9499549/ /pubmed/36095209 http://dx.doi.org/10.1073/pnas.2122969119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Dai, Liufeng
Wang, Baojie
Wang, Ting
Meyer, Etienne H.
Kettel, Valentin
Hoffmann, Natalie
McFarlane, Heather E.
Li, Shalan
Wu, Xuna
Picard, Kelsey L.
Giavalisco, Patrick
Persson, Staffan
Zhang, Yi
The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title_full The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title_fullStr The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title_full_unstemmed The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title_short The TOR complex controls ATP levels to regulate actin cytoskeleton dynamics in Arabidopsis
title_sort tor complex controls atp levels to regulate actin cytoskeleton dynamics in arabidopsis
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9499549/
https://www.ncbi.nlm.nih.gov/pubmed/36095209
http://dx.doi.org/10.1073/pnas.2122969119
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