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Cytoskeletal organization in isolated plant cells under geometry control

Durand-Smet, Pauline ; Spelman, Tamsin A. ; Meyerowitz, Elliot M. and Jönsson, Henrik LU (2020) In Proceedings of the National Academy of Sciences of the United States of America 117(29). p.17399-17408
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... (More)

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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author
; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Actin, Cell geometry, Cytoskeleton, Microtubules, Plant cells
in
Proceedings of the National Academy of Sciences of the United States of America
volume
117
issue
29
pages
10 pages
publisher
National Academy of Sciences
external identifiers
  • pmid:32641513
  • scopus:85088881126
ISSN
0027-8424
DOI
10.1073/pnas.2003184117
language
English
LU publication?
yes
id
6dd2f6f5-bb52-4ff5-a2dc-3d2871a1a08d
date added to LUP
2021-01-08 14:26:02
date last changed
2024-06-27 05:29:51
@article{6dd2f6f5-bb52-4ff5-a2dc-3d2871a1a08d,
  abstract     = {{<p>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.</p>}},
  author       = {{Durand-Smet, Pauline and Spelman, Tamsin A. and Meyerowitz, Elliot M. and Jönsson, Henrik}},
  issn         = {{0027-8424}},
  keywords     = {{Actin; Cell geometry; Cytoskeleton; Microtubules; Plant cells}},
  language     = {{eng}},
  number       = {{29}},
  pages        = {{17399--17408}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences of the United States of America}},
  title        = {{Cytoskeletal organization in isolated plant cells under geometry control}},
  url          = {{http://dx.doi.org/10.1073/pnas.2003184117}},
  doi          = {{10.1073/pnas.2003184117}},
  volume       = {{117}},
  year         = {{2020}},
}