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

Sampathkumar, Arun; Krupinski, Pawel LU ; Wightman, Raymond; Milani, Pascale; Berquand, Alexandre; Boudaoud, Arezki; Hamant, Olivier; Jönsson, Henrik LU and Meyerowitz, Elliot M. (2014) In eLife 3.
Abstract
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... (More)
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. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
eLife
volume
3
publisher
eLife Sciences Publications LTD.
external identifiers
  • wos:000334352900001
  • scopus:84899646073
ISSN
2050-084X
DOI
10.7554/eLife.01967.001
language
English
LU publication?
yes
id
2a8d26d1-4833-4b23-8962-1a37f6d9e8ab (old id 4439516)
date added to LUP
2014-05-20 12:54:31
date last changed
2017-10-01 04:11:35
@article{2a8d26d1-4833-4b23-8962-1a37f6d9e8ab,
  abstract     = {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.},
  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.},
  issn         = {2050-084X},
  language     = {eng},
  publisher    = {eLife Sciences Publications LTD.},
  series       = {eLife},
  title        = {Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells},
  url          = {http://dx.doi.org/10.7554/eLife.01967.001},
  volume       = {3},
  year         = {2014},
}