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The self-organization of plant microtubules in three dimensions enable stable cortical localization and sensitivity to external cues

Vincent Mirabet, View ORCID ProfilePawel Krupinski, Olivier Hamant, View ORCID ProfileElliot M Meyerowitz, View ORCID ProfileHenrik Jönsson, View ORCID ProfileArezki Boudaoud
doi: https://doi.org/10.1101/210138
Vincent Mirabet
1Reproduction et Développement des Plantes, Univ. Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA,F-69364 Lyon, France.
3Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge CB2 1LR, UK.
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  • For correspondence: vincent.mirabet@gmail.com arezki.boudaoud@ens-lyon.fr
Pawel Krupinski
2Computational Biology and Biological Physics Group, Department of Theoretical Physics, Lund University, S-221 00 Lund, Sweden.
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Olivier Hamant
1Reproduction et Développement des Plantes, Univ. Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA,F-69364 Lyon, France.
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Elliot M Meyerowitz
4Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA.
5Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125, USA.
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Henrik Jönsson
2Computational Biology and Biological Physics Group, Department of Theoretical Physics, Lund University, S-221 00 Lund, Sweden.
3Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge CB2 1LR, UK.
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Arezki Boudaoud
1Reproduction et Développement des Plantes, Univ. Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA,F-69364 Lyon, France.
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  • For correspondence: vincent.mirabet@gmail.com arezki.boudaoud@ens-lyon.fr
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Abstract

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 in the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Using a computational model of microtubules enclosed in a three-dimensional space, We show that the microtubule network has spontaneous configurations that could explain many experimental observations without resorting to specific regulation. In particular, we find that the preferred localization of microtubules at the cortex emerges from directional persistence of the microtubules, combined with their growth mode. We identified microtubule parameters that seem relatively insensitive to cell shape, such as length or number. In contrast, microtubule array anisotropy depends strongly on local curvature of the cell surface and global orientation follows robustly the longest axis of the cell. Lastly, we found that 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, it easily reaches stable global configurations.

Author summary Plants exhibit an astonishing diversity in architecture and shape. A key to such diversity is the ability of their cells to coordinate and grow to reach a broad spectrum of sizes and shapes. Cell growth in plants is guided by the microtubule cytoskeleton. Here, we seek to understand how microtubules self-organize close to the cell surface. We build upon previous two-dimensional models and we consider microtubules as lines growing in three dimensions, accounting for interactions between microtubules or between microtubules and the cell surface. We show that microtubule arrays are able to adapt to various cell shapes and to reorient in response to factors such as signals or environment. Altogether, our results help to understand how the microtubule cytoskeleton contributes to the diversity of plant shapes and to how these shapes adapt to environment.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 27, 2017.
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The self-organization of plant microtubules in three dimensions enable stable cortical localization and sensitivity to external cues
Vincent Mirabet, Pawel Krupinski, Olivier Hamant, Elliot M Meyerowitz, Henrik Jönsson, Arezki Boudaoud
bioRxiv 210138; doi: https://doi.org/10.1101/210138
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The self-organization of plant microtubules in three dimensions enable stable cortical localization and sensitivity to external cues
Vincent Mirabet, Pawel Krupinski, Olivier Hamant, Elliot M Meyerowitz, Henrik Jönsson, Arezki Boudaoud
bioRxiv 210138; doi: https://doi.org/10.1101/210138

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