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The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues

Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy of the cell wall. Here we analyze how, i...

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Autores principales: Mirabet, Vincent, Krupinski, Pawel, Hamant, Olivier, Meyerowitz, Elliot M., Jönsson, Henrik, Boudaoud, Arezki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834207/
https://www.ncbi.nlm.nih.gov/pubmed/29462151
http://dx.doi.org/10.1371/journal.pcbi.1006011
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author Mirabet, Vincent
Krupinski, Pawel
Hamant, Olivier
Meyerowitz, Elliot M.
Jönsson, Henrik
Boudaoud, Arezki
author_facet Mirabet, Vincent
Krupinski, Pawel
Hamant, Olivier
Meyerowitz, Elliot M.
Jönsson, Henrik
Boudaoud, Arezki
author_sort Mirabet, Vincent
collection PubMed
description Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy of the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Building upon previous models that confined microtubules to the cell surface, we introduce an agent model of microtubules enclosed in a three-dimensional volume. We show that the microtubule network has spontaneous aligned configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred cortical localization of microtubules emerges from directional persistence of the microtubules, and their interactions with each other and with the stiff wall. We also identify microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we find that geometric cues may be overcome, as the network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, easily reaching stable global configurations.
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spelling pubmed-58342072018-03-23 The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues Mirabet, Vincent Krupinski, Pawel Hamant, Olivier Meyerowitz, Elliot M. Jönsson, Henrik Boudaoud, Arezki PLoS Comput Biol Research Article Many cell functions rely on the ability of microtubules to self-organize as complex networks. In plants, cortical microtubules are essential to determine cell shape as they guide the deposition of cellulose microfibrils, and thus control mechanical anisotropy of the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Building upon previous models that confined microtubules to the cell surface, we introduce an agent model of microtubules enclosed in a three-dimensional volume. We show that the microtubule network has spontaneous aligned configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred cortical localization of microtubules emerges from directional persistence of the microtubules, and their interactions with each other and with the stiff wall. We also identify microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we find that geometric cues may be overcome, as the network is capable of reorienting toward weak external directional cues. Altogether our simulations show that the microtubule network is a good transducer of weak external polarity, while at the same time, easily reaching stable global configurations. Public Library of Science 2018-02-20 /pmc/articles/PMC5834207/ /pubmed/29462151 http://dx.doi.org/10.1371/journal.pcbi.1006011 Text en © 2018 Mirabet et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Mirabet, Vincent
Krupinski, Pawel
Hamant, Olivier
Meyerowitz, Elliot M.
Jönsson, Henrik
Boudaoud, Arezki
The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title_full The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title_fullStr The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title_full_unstemmed The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title_short The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
title_sort self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834207/
https://www.ncbi.nlm.nih.gov/pubmed/29462151
http://dx.doi.org/10.1371/journal.pcbi.1006011
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