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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

Mirabet, Vincent and Krupinski, Pawel and Hamant, Olivier and Meyerowitz, Elliot M. and Jönsson, Henrik and Boudaoud, Arezki (2018) The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues. PLOS Computational Biology, 14 (2). Art. No. e1006011. ISSN 1553-7358. PMCID PMC5834207. https://resolver.caltech.edu/CaltechAUTHORS:20180227-153456402

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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 of the cell wall. Here we analyze how, in turn, cell shape may influence microtubule behavior. Buidling 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 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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pcbi.1006011DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834207/PubMed CentralArticle
https://doi.org/10.1371/journal.pcbi.1006011.s001DOIS1 Fig.
https://doi.org/10.1371/journal.pcbi.1006011.s002DOIS2 Fig.
https://doi.org/10.1371/journal.pcbi.1006011.s003DOIS1 Video
https://doi.org/10.1371/journal.pcbi.1006011.s004DOIS2 Video
https://doi.org/10.1101/210138DOIDiscussion Paper
ORCID:
AuthorORCID
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Alternate Title:The self-organization of plant microtubules in three dimensions enables stable cortical localization and sensitivity to external cues
Additional Information:© 2018 Mirabet et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: July 25, 2017; Accepted: January 31, 2018; Published: February 20, 2018. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. This work was supported by Agence Nationale de la Recherche (http://www.agence-nationale-recherche.fr, grants ANR-10-BLAN-1516 to OH and 12-BSV2-0023-02 to AB), by the European Research Council (https://erc.europa.eu, grants #307387 to AB and #615739 to OH), and by the Gatsby Charitable Foundation (http://www.gatsby.org.uk, grants GAT3395/DAA to EMM and GAT3395-PR4 to HJ). EMM also acknowledges support from the Howard Hughes Medical Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have declared that no competing interests exist. We thank the members of RDP and Sainsbury laboratories for discussions and support. Author Contributions: Conceptualization: Vincent Mirabet, Olivier Hamant, Elliot M. Meyerowitz, Henrik JoÈnsson, Arezki Boudaoud. Formal analysis: Vincent Mirabet. Funding acquisition: Olivier Hamant, Elliot M. Meyerowitz, Henrik JoÈnsson, Arezki Boudaoud. Investigation: Vincent Mirabet. Methodology: Vincent Mirabet. Resources: Pawel Krupinski. Software: Vincent Mirabet. Supervision: Arezki Boudaoud. Validation: Vincent Mirabet. Visualization: Vincent Mirabet. Writing ± original draft: Vincent Mirabet, Olivier Hamant, Arezki Boudaoud. Writing ± review & editing: Vincent Mirabet, Olivier Hamant, Elliot M. Meyerowitz, Henrik JoÈnsson, Arezki Boudaoud.
Funders:
Funding AgencyGrant Number
Agence Nationale pour la Recherche (ANR)ANR-10-BLAN-1516
Agence Nationale pour la Recherche (ANR)ANR-12-BSV2-0023-02
European Research Council (ERC)307387
European Research Council (ERC)615739
Gatsby Charitable FoundationGAT3395/DAA
Gatsby Charitable FoundationGAT3395-PR4
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Issue or Number:2
PubMed Central ID:PMC5834207
Record Number:CaltechAUTHORS:20180227-153456402
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180227-153456402
Official Citation:Mirabet V, Krupinski P, Hamant O, Meyerowitz EM, JoÈnsson H, Boudaoud A (2018) The self-organization of plant microtubules inside the cell volume yields their cortical localization, stable alignment, and sensitivity to external cues. PLoS Comput Biol 14(2): e1006011. https://doi. org/10.1371/journal.pcbi.1006011
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:84976
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:28 Feb 2018 01:08
Last Modified:03 Oct 2019 19:25

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