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

Author:

Dai Liufeng1ORCID,Wang Baojie1,Wang Ting1ORCID,Meyer Etienne H.2ORCID,Kettel Valentin2ORCID,Hoffmann Natalie3ORCID,McFarlane Heather E.3ORCID,Li Shalan4,Wu Xuna4ORCID,Picard Kelsey L.56,Giavalisco Patrick7,Persson Staffan58910ORCID,Zhang Yi111ORCID

Affiliation:

1. Key Laboratory of Cell Proliferation and Regulation Biology of Ministry of Education, College of Life Science, Beijing Normal University, Beijing 100875, China

2. Martin-Luther-University Halle-Wittenberg, Institute of Plant Physiology, 06120 Halle (Saale), Germany

3. Department of Cell & Systems Biology, University of Toronto, Toronto, ON M5S 3G5, Canada

4. State Key Laboratory of Conservation and Utilization of Bio-resources in Yunnan, Center for Life Sciences, School of Life Sciences, Yunnan University, Kunming 650091, China

5. School of Biosciences, University of Melbourne, Parkville 3010 VIC, Melbourne, Australia

6. School of Natural Sciences, University of Tasmania, Hobart 7001, TAS, Australia

7. Metabolomics Core Facility, Max Planck Institute for Biology of Ageing, 50931 Cologne, Germany

8. Department of Plant and Environmental Sciences, University of Copenhagen, 1871 Frederiksberg C, Denmark

9. Copenhagen Plant Science Center, University of Copenhagen, 1871 Frederiksberg C, Denmark

10. Joint International Research Laboratory of Metabolic & Developmental Sciences, State Key Laboratory of Hybrid Rice, SJTU-University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China

11. Max-Planck Institute for Molecular Plant Physiology, Am Muehlenberg 1, 14476 Potsdam, Germany

Abstract

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.

Funder

National Natural Science Foundation of China

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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