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Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana

In plants, the robust maintenance of tissue structure is crucial to supporting its functionality. The multi-layered shoot apical meristem (SAM) of Arabidopsis, containing stem cells, is an approximately radially symmetric tissue whose shape and structure is maintained throughout the life of the plan...

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Autores principales: Michael, Christian, Banwarth-Kuhn, Mikahl, Rodriguez, Kevin, Ta, Calvin-Khang, Roy-Chowdhury, Amit, Chen, Weitao, Venugopala Reddy, G., Alber, Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10244971/
https://www.ncbi.nlm.nih.gov/pubmed/37282588
http://dx.doi.org/10.1098/rsif.2023.0173
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author Michael, Christian
Banwarth-Kuhn, Mikahl
Rodriguez, Kevin
Ta, Calvin-Khang
Roy-Chowdhury, Amit
Chen, Weitao
Venugopala Reddy, G.
Alber, Mark
author_facet Michael, Christian
Banwarth-Kuhn, Mikahl
Rodriguez, Kevin
Ta, Calvin-Khang
Roy-Chowdhury, Amit
Chen, Weitao
Venugopala Reddy, G.
Alber, Mark
author_sort Michael, Christian
collection PubMed
description In plants, the robust maintenance of tissue structure is crucial to supporting its functionality. The multi-layered shoot apical meristem (SAM) of Arabidopsis, containing stem cells, is an approximately radially symmetric tissue whose shape and structure is maintained throughout the life of the plant. In this paper, a new biologically calibrated pseudo-three-dimensional (P3D) computational model of a longitudinal section of the SAM is developed. It includes anisotropic expansion and division of cells out of the cross-section plane, as well as representation of tension experienced by the SAM epidermis. Results from the experimentally calibrated P3D model provide new insights into maintenance of the structure of the SAM epidermal cell monolayer under tension and quantify dependence of epidermal and subepidermal cell anisotropy on the amount of tension. Moreover, the model simulations revealed that out-of-plane cell growth is important in offsetting cell crowding and regulating mechanical stresses experienced by tunica cells. Predictive model simulations show that tension-determined cell division plane orientation in the apical corpus may be regulating cell and tissue shape distributions needed for maintaining structure of the wild-type SAM. This suggests that cells' responses to local mechanical cues may serve as a mechanism to regulate cell- and tissue-scale patterning.
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spelling pubmed-102449712023-06-08 Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana Michael, Christian Banwarth-Kuhn, Mikahl Rodriguez, Kevin Ta, Calvin-Khang Roy-Chowdhury, Amit Chen, Weitao Venugopala Reddy, G. Alber, Mark J R Soc Interface Life Sciences–Mathematics interface In plants, the robust maintenance of tissue structure is crucial to supporting its functionality. The multi-layered shoot apical meristem (SAM) of Arabidopsis, containing stem cells, is an approximately radially symmetric tissue whose shape and structure is maintained throughout the life of the plant. In this paper, a new biologically calibrated pseudo-three-dimensional (P3D) computational model of a longitudinal section of the SAM is developed. It includes anisotropic expansion and division of cells out of the cross-section plane, as well as representation of tension experienced by the SAM epidermis. Results from the experimentally calibrated P3D model provide new insights into maintenance of the structure of the SAM epidermal cell monolayer under tension and quantify dependence of epidermal and subepidermal cell anisotropy on the amount of tension. Moreover, the model simulations revealed that out-of-plane cell growth is important in offsetting cell crowding and regulating mechanical stresses experienced by tunica cells. Predictive model simulations show that tension-determined cell division plane orientation in the apical corpus may be regulating cell and tissue shape distributions needed for maintaining structure of the wild-type SAM. This suggests that cells' responses to local mechanical cues may serve as a mechanism to regulate cell- and tissue-scale patterning. The Royal Society 2023-06-07 /pmc/articles/PMC10244971/ /pubmed/37282588 http://dx.doi.org/10.1098/rsif.2023.0173 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Life Sciences–Mathematics interface
Michael, Christian
Banwarth-Kuhn, Mikahl
Rodriguez, Kevin
Ta, Calvin-Khang
Roy-Chowdhury, Amit
Chen, Weitao
Venugopala Reddy, G.
Alber, Mark
Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title_full Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title_fullStr Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title_full_unstemmed Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title_short Role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of Arabidopsis thaliana
title_sort role of turgor-pressure induced boundary tension in the maintenance of the shoot apical meristem of arabidopsis thaliana
topic Life Sciences–Mathematics interface
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10244971/
https://www.ncbi.nlm.nih.gov/pubmed/37282588
http://dx.doi.org/10.1098/rsif.2023.0173
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