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

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...

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Autores principales: Bonfanti, Alessandra, Smithers, Euan Thomas, Bourdon, Matthieu, Guyon, Alex, Carella, Philip, Carter, Ross, Wightman, Raymond, Schornack, Sebastian, Jönsson, Henrik, Robinson, Sarah
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10576037/
https://www.ncbi.nlm.nih.gov/pubmed/37782806
http://dx.doi.org/10.1073/pnas.2302985120
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author Bonfanti, Alessandra
Smithers, Euan Thomas
Bourdon, Matthieu
Guyon, Alex
Carella, Philip
Carter, Ross
Wightman, Raymond
Schornack, Sebastian
Jönsson, Henrik
Robinson, Sarah
author_facet Bonfanti, Alessandra
Smithers, Euan Thomas
Bourdon, Matthieu
Guyon, Alex
Carella, Philip
Carter, Ross
Wightman, Raymond
Schornack, Sebastian
Jönsson, Henrik
Robinson, Sarah
author_sort Bonfanti, Alessandra
collection PubMed
description 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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spelling pubmed-105760372023-10-15 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 Robinson, Sarah Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2023-10-02 2023-10-10 /pmc/articles/PMC10576037/ /pubmed/37782806 http://dx.doi.org/10.1073/pnas.2302985120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Bonfanti, Alessandra
Smithers, Euan Thomas
Bourdon, Matthieu
Guyon, Alex
Carella, Philip
Carter, Ross
Wightman, Raymond
Schornack, Sebastian
Jönsson, Henrik
Robinson, Sarah
Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title_full Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title_fullStr Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title_full_unstemmed Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title_short Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves
title_sort stiffness transitions in new walls post-cell division differ between marchantia polymorpha gemmae and arabidopsis thaliana leaves
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10576037/
https://www.ncbi.nlm.nih.gov/pubmed/37782806
http://dx.doi.org/10.1073/pnas.2302985120
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