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Cytoskeletal organization in isolated plant cells under geometry control

Durand-Smet, Pauline and Spelman, Tamsin A. and Meyerowitz, Elliot M. and Jönsson, Henrik (2020) Cytoskeletal organization in isolated plant cells under geometry control. Proceedings of the National Academy of Sciences of the United States of America, 117 (29). pp. 17399-17408. ISSN 0027-8424. PMCID PMC7382239. https://resolver.caltech.edu/CaltechAUTHORS:20191001-104800188

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Abstract

The cytoskeleton plays a key role in establishing robust cell shape. In animals, it is well established that cell shape can also influence cytoskeletal organization. Cytoskeletal proteins are well conserved between animal and plant kingdoms; nevertheless, because plant cells exhibit major structural differences to animal cells, the question arises whether the plant cytoskeleton also responds to geometrical cues. Recent numerical simulations predicted that a geometry-based rule is sufficient to explain the microtubule (MT) organization observed in cells. Due to their high flexural rigidity and persistence length of the order of a few millimeters, MTs are rigid over cellular dimensions and are thus expected to align along their long axis if constrained in specific geometries. This hypothesis remains to be tested in cellulo. Here, we explore the relative contribution of geometry to the final organization of actin and MT cytoskeletons in single plant cells of Arabidopsis thaliana. We show that the cytoskeleton aligns with the long axis of the cells. We find that actin organization relies on MTs but not the opposite. We develop a model of self-organizing MTs in three dimensions, which predicts the importance of MT severing, which we confirm experimentally. This work is a first step toward assessing quantitatively how cellular geometry contributes to the control of cytoskeletal organization in living plant cells.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1073/pnas.2003184117DOIArticle
https://www.pnas.org/content/suppl/2020/07/03/2003184117.DCSupplementalPublisherSupporting Information
https://doi.org/10.1101/784595DOIDiscussion Paper
https://gitlab.com/slcu/teamHJ/publications/durand_etal_2019Related ItemScripts related to the manuscript "Cytoskeletal organization in isolated plant cells under geometry control"
https://gitlab.com/slcu/teamHJ/tubulatonRelated ItemCode for simulations of individual Microtubules in 3D and constrained by a meshed description of a cell membrane
https://doi.org/10.17863/CAM.51754Related ItemData
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7382239/PubMed CentralArticle
ORCID:
AuthorORCID
Durand-Smet, Pauline0000-0003-0647-5878
Spelman, Tamsin A.0000-0002-4991-7931
Meyerowitz, Elliot M.0000-0003-4798-5153
Jönsson, Henrik0000-0003-2340-588X
Additional Information:© 2020 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY). Contributed by Elliot M. Meyerowitz, May 19, 2020 (sent for review February 20, 2020; reviewed by Naomi Nakayama and Timothy E. Saunders). PNAS first published July 8, 2020. We thank all members from E.M.M. and H.J. groups as well as Sarah Robinson, Olivier Hamant, Arun Sampathkumar, and Francois Nedelec for stimulating discussions. P.D.-S. was funded by global individual fellowship Marie Sklodowska-Curie (PlantCellMech H2020 Grant 703802), and T.A.S. and H.J. by Gatsby (GAT3395/PR4B) and Human Frontier Science Program Organization (Grant RGP0009/2018). The work in the E.M.M. laboratory at the California Institute of Technology was partially funded by the Howard Hughes Medical Institute. Author contributions: P.D.-S., T.A.S., E.M.M., and H.J. designed research; P.D.-S. and T.A.S. performed research; P.D.-S. and T.A.S. contributed new reagents/analytic tools; P.D.-S., T.A.S., E.M.M., and H.J. analyzed data; and P.D.-S., E.M.M., and H.J. wrote the paper. Reviewers: N.N., Imperial College London; and T.E.S., National University of Singapore. The authors declare no competing interest. Data deposition: Original confocal data have been deposited to the University of Cambridge Research Data Repository (https://doi.org/10.17863/CAM.51754); data for plotting the figures as well as code used for the analysis and 3D MT simulations have been deposited to the Sainsbury Laboratory GitLab repository (https://gitlab.com/slcu/teamhj/publications/durand_etal_2019; https://gitlab.com/slcu/teamhj/Tubulaton). This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2003184117/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Marie Curie Fellowship703802
Gatsby Charitable FoundationGAT3395/PR4
Human Frontier Science ProgramRGP0009/2018
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:cytoskeleton; microtubules; plant cells; actin; cell geometry
Issue or Number:29
PubMed Central ID:PMC7382239
Record Number:CaltechAUTHORS:20191001-104800188
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191001-104800188
Official Citation:Cytoskeletal organization in isolated plant cells under geometry control. Pauline Durand-Smet, Tamsin A. Spelman, Elliot M. Meyerowitz, Henrik Jönsson. Proceedings of the National Academy of Sciences Jul 2020, 117 (29) 17399-17408; DOI: 10.1073/pnas.2003184117
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:98981
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:01 Oct 2019 20:37
Last Modified:31 Jul 2020 15:41

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