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

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. (2014) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife, 2014 (3). Art. No. e01967. ISSN 2050-084X. PMCID PMC3985187. doi:10.7554/eLife.01967.001. https://resolver.caltech.edu/CaltechAUTHORS:20140422-144226850

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.7554/eLife.01967.001DOIArticle
http://elifesciences.org/content/3/e01967PublisherArticle
http://elifesciences.org/content/3/e01967/DC1PublisherSupplementary File
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3985187/PubMed CentralArticle
ORCID:
AuthorORCID
Sampathkumar, Arun0000-0003-1703-0137
Wightman, Raymond0000-0003-1295-4875
Jönsson, Henrik0000-0003-2340-588X
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2014, Sampathkumar et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 27 November 2013; Accepted: 07 March 2014; Published: 16 April 2014. We would like to thank An Yan, Division of Biology, California Institute of Technology for his comments on the manuscript and Nathan Hervieux, ENS Lyon, for help with quantification of nematic tensor values in large scale laceration experiments. This work is supported by the Gatsby Charitable Foundation to HJ and EMM, the Department of Energy Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences and Biosciences, of the US Department of Energy [DE-FG02-88ER13873] to EMM, the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through Grant GBMF3406) to EMM, Agence Nationale de la Recherche ANR-10-BLAN-1516 ‘Mechastem’ to OH, the European Research Council starting grant (PhyMorph, #307387) to AB and by the Swedish Research Council and the Crafoord Foundation to HJ. These authors contributed equally to this work: Arun Sampathkumar; Pawel Krupinski. Author contributions: AS, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article PK, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article OH, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article RW, Acquisition of data, Analysis and interpretation of data PM, Acquisition of data, Analysis and interpretation of data AB, Acquisition of data AB, Conception and design, Drafting or revising the article HJ, Conception and design, Analysis and interpretation of data, Drafting or revising the article EMM, Conception and design, Analysis and interpretation of data, Drafting or revising the article The authors declare that no competing interests exist. Funding: Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation GBMF3406 Elliot M Meyerowitz Gatsby Charitable Foundation Henrik Jönsson Elliot M Meyerowitz US Department of Energy DE-FG02-88ER13873 Elliot M Meyerowitz Agence Nationale de la Recherche ANR-10-BLAN-1516 Olivier Hamant European Research Council 307387 Arezki Boudaoud Swedish Research Council Henrik Jönsson Crafoord Foundation Henrik Jönsson The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Funders:
Funding AgencyGrant Number
Gatsby Charitable FoundationUNSPECIFIED
Department of Energy (DOE)DE-FG02-88ER13873
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
Agence Nationale de la Recherche (ANR)ANR-10-BLAN-1516
European Research Council (ERC)307387
Swedish Research CouncilUNSPECIFIED
Crafoord FoundationUNSPECIFIED
Issue or Number:3
PubMed Central ID:PMC3985187
DOI:10.7554/eLife.01967.001
Record Number:CaltechAUTHORS:20140422-144226850
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140422-144226850
Official Citation:Sampathkumar et al. eLife 2014;3:e01967
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:45121
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Apr 2014 19:57
Last Modified:10 Nov 2021 17:00

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