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Cytoskeletal organization in isolated plant cells under geometry control

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...

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Autores principales: Durand-Smet, Pauline, Spelman, Tamsin A., Meyerowitz, Elliot M., Jönsson, Henrik
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7382239/
https://www.ncbi.nlm.nih.gov/pubmed/32641513
http://dx.doi.org/10.1073/pnas.2003184117
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author Durand-Smet, Pauline
Spelman, Tamsin A.
Meyerowitz, Elliot M.
Jönsson, Henrik
author_facet Durand-Smet, Pauline
Spelman, Tamsin A.
Meyerowitz, Elliot M.
Jönsson, Henrik
author_sort Durand-Smet, Pauline
collection PubMed
description 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.
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spelling pubmed-73822392020-07-30 Cytoskeletal organization in isolated plant cells under geometry control Durand-Smet, Pauline Spelman, Tamsin A. Meyerowitz, Elliot M. Jönsson, Henrik Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2020-07-21 2020-07-08 /pmc/articles/PMC7382239/ /pubmed/32641513 http://dx.doi.org/10.1073/pnas.2003184117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Durand-Smet, Pauline
Spelman, Tamsin A.
Meyerowitz, Elliot M.
Jönsson, Henrik
Cytoskeletal organization in isolated plant cells under geometry control
title Cytoskeletal organization in isolated plant cells under geometry control
title_full Cytoskeletal organization in isolated plant cells under geometry control
title_fullStr Cytoskeletal organization in isolated plant cells under geometry control
title_full_unstemmed Cytoskeletal organization in isolated plant cells under geometry control
title_short Cytoskeletal organization in isolated plant cells under geometry control
title_sort cytoskeletal organization in isolated plant cells under geometry control
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7382239/
https://www.ncbi.nlm.nih.gov/pubmed/32641513
http://dx.doi.org/10.1073/pnas.2003184117
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AT jonssonhenrik cytoskeletalorganizationinisolatedplantcellsundergeometrycontrol