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Title: Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells

Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.
Authors:
; ; ; ; ; ; ; ;
Publication Date:
Grant/Contract Number:
FG02-88ER13873
Type:
Published Article
Journal Name:
eLife
Additional Journal Information:
Journal Name: eLife Journal Volume: 3; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
OSTI Identifier:
1197663
Alternate Identifier(s):
OSTI ID: 1197668

Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, and Meyerowitz, Elliot M. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. United States: N. p., Web. doi:10.7554/eLife.01967.
Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, & Meyerowitz, Elliot M. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. United States. doi:10.7554/eLife.01967.
Sampathkumar, Arun, Krupinski, Pawel, Wightman, Raymond, Milani, Pascale, Berquand, Alexandre, Boudaoud, Arezki, Hamant, Olivier, Jönsson, Henrik, and Meyerowitz, Elliot M. 2014. "Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells". United States. doi:10.7554/eLife.01967.
@article{osti_1197663,
title = {Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells},
author = {Sampathkumar, Arun and Krupinski, Pawel and Wightman, Raymond and Milani, Pascale and Berquand, Alexandre and Boudaoud, Arezki and Hamant, Olivier and Jönsson, Henrik and Meyerowitz, Elliot M.},
abstractNote = {Although it is a central question in biology, how cell shape controls intracellular dynamics largely remains an open question. Here, we show that the shape of Arabidopsis pavement cells creates a stress pattern that controls microtubule orientation, which then guides cell wall reinforcement. Live-imaging, combined with modeling of cell mechanics, shows that microtubules align along the maximal tensile stress direction within the cells, and atomic force microscopy demonstrates that this leads to reinforcement of the cell wall parallel to the microtubules. This feedback loop is regulated: cell-shape derived stresses could be overridden by imposed tissue level stresses, showing how competition between subcellular and supracellular cues control microtubule behavior. Furthermore, at the microtubule level, we identified an amplification mechanism in which mechanical stress promotes the microtubule response to stress by increasing severing activity. These multiscale feedbacks likely contribute to the robustness of microtubule behavior in plant epidermis.},
doi = {10.7554/eLife.01967},
journal = {eLife},
number = ,
volume = 3,
place = {United States},
year = {2014},
month = {4}
}

Works referenced in this record:

Matrix Elasticity Directs Stem Cell Lineage Specification
journal, August 2006