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Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

Bonfanti, Alessandra ; Smithers, Euan Thomas ; Bourdon, Matthieu ; Guyon, Alex ; Carella, Philip ; Carter, Ross ; Wightman, Raymond ; Schornack, Sebastian ; Jönsson, Henrik LU and Robinson, Sarah (2023) In Proceedings of the National Academy of Sciences of the United States of America 120(41).
Abstract

Plant morphogenesis is governed by the mechanics of the cell wall—a stiff and thin polymeric box that encloses the cells. The cell wall is a highly dynamic composite material. New cell walls are added during cell division. As the cells continue to grow, the properties of cell walls are modulated to undergo significant changes in shape and size without breakage. Spatial and temporal variations in cell wall mechanical properties have been observed. However, how they relate to cell division remains an outstanding question. Here, we combine time-lapse imaging with local mechanical measurements via atomic force microscopy to systematically map the cell wall’s age and growth, with their stiffness. We make use of two systems, Marchantia... (More)

Plant morphogenesis is governed by the mechanics of the cell wall—a stiff and thin polymeric box that encloses the cells. The cell wall is a highly dynamic composite material. New cell walls are added during cell division. As the cells continue to grow, the properties of cell walls are modulated to undergo significant changes in shape and size without breakage. Spatial and temporal variations in cell wall mechanical properties have been observed. However, how they relate to cell division remains an outstanding question. Here, we combine time-lapse imaging with local mechanical measurements via atomic force microscopy to systematically map the cell wall’s age and growth, with their stiffness. We make use of two systems, Marchantia polymorpha gemmae, and Arabidopsis thaliana leaves. We first characterize the growth and cell division of M. polymorpha gemmae. We then demonstrate that cell division in M. polymorpha gemmae results in the generation of a temporary stiffer and slower-growing new wall. In contrast, this transient phenomenon is absent in A. thaliana leaves. We provide evidence that this different temporal behavior has a direct impact on the local cell geometry via changes in the junction angle. These results are expected to pave the way for developing more realistic plant morphogenetic models and to advance the study into the impact of cell division on tissue growth.

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organization
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type
Contribution to journal
publication status
published
subject
in
Proceedings of the National Academy of Sciences of the United States of America
volume
120
issue
41
article number
e2302985120
publisher
National Academy of Sciences
external identifiers
  • pmid:37782806
  • scopus:85173038408
ISSN
0027-8424
DOI
10.1073/pnas.2302985120
language
English
LU publication?
yes
additional info
Publisher Copyright: Copyright © 2023 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
id
3442e803-1e80-4318-981e-c4024445811b
date added to LUP
2023-12-04 16:37:42
date last changed
2024-04-17 12:52:45
@article{3442e803-1e80-4318-981e-c4024445811b,
  abstract     = {{<p>Plant morphogenesis is governed by the mechanics of the cell wall—a stiff and thin polymeric box that encloses the cells. The cell wall is a highly dynamic composite material. New cell walls are added during cell division. As the cells continue to grow, the properties of cell walls are modulated to undergo significant changes in shape and size without breakage. Spatial and temporal variations in cell wall mechanical properties have been observed. However, how they relate to cell division remains an outstanding question. Here, we combine time-lapse imaging with local mechanical measurements via atomic force microscopy to systematically map the cell wall’s age and growth, with their stiffness. We make use of two systems, Marchantia polymorpha gemmae, and Arabidopsis thaliana leaves. We first characterize the growth and cell division of M. polymorpha gemmae. We then demonstrate that cell division in M. polymorpha gemmae results in the generation of a temporary stiffer and slower-growing new wall. In contrast, this transient phenomenon is absent in A. thaliana leaves. We provide evidence that this different temporal behavior has a direct impact on the local cell geometry via changes in the junction angle. These results are expected to pave the way for developing more realistic plant morphogenetic models and to advance the study into the impact of cell division on tissue growth.</p>}},
  author       = {{Bonfanti, Alessandra and Smithers, Euan Thomas and Bourdon, Matthieu and Guyon, Alex and Carella, Philip and Carter, Ross and Wightman, Raymond and Schornack, Sebastian and Jönsson, Henrik and Robinson, Sarah}},
  issn         = {{0027-8424}},
  language     = {{eng}},
  month        = {{10}},
  number       = {{41}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences of the United States of America}},
  title        = {{Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves}},
  url          = {{http://dx.doi.org/10.1073/pnas.2302985120}},
  doi          = {{10.1073/pnas.2302985120}},
  volume       = {{120}},
  year         = {{2023}},
}