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Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem

The control of cell position and division act in concert to dictate multicellular organization in tissues and organs. How these processes shape global order and molecular movement across organs is an outstanding problem in biology. Using live 3D imaging and computational analyses, we extracted netwo...

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Autores principales: Jackson, Matthew D.B., Duran-Nebreda, Salva, Kierzkowski, Daniel, Strauss, Soeren, Xu, Hao, Landrein, Benoit, Hamant, Olivier, Smith, Richard S., Johnston, Iain G., Bassel, George W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345583/
https://www.ncbi.nlm.nih.gov/pubmed/30660611
http://dx.doi.org/10.1016/j.cels.2018.12.009
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author Jackson, Matthew D.B.
Duran-Nebreda, Salva
Kierzkowski, Daniel
Strauss, Soeren
Xu, Hao
Landrein, Benoit
Hamant, Olivier
Smith, Richard S.
Johnston, Iain G.
Bassel, George W.
author_facet Jackson, Matthew D.B.
Duran-Nebreda, Salva
Kierzkowski, Daniel
Strauss, Soeren
Xu, Hao
Landrein, Benoit
Hamant, Olivier
Smith, Richard S.
Johnston, Iain G.
Bassel, George W.
author_sort Jackson, Matthew D.B.
collection PubMed
description The control of cell position and division act in concert to dictate multicellular organization in tissues and organs. How these processes shape global order and molecular movement across organs is an outstanding problem in biology. Using live 3D imaging and computational analyses, we extracted networks capturing cellular connectivity dynamics across the Arabidopsis shoot apical meristem (SAM) and topologically analyzed the local and global properties of cellular architecture. Locally generated cell division rules lead to the emergence of global tissue-scale organization of the SAM, facilitating robust global communication. Cells that lie upon more shorter paths have an increased propensity to divide, with division plane placement acting to limit the number of shortest paths their daughter cells lie upon. Cell shape heterogeneity and global cellular organization requires KATANIN, providing a multiscale link between cell geometry, mechanical cell-cell interactions, and global tissue order.
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spelling pubmed-63455832019-01-28 Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem Jackson, Matthew D.B. Duran-Nebreda, Salva Kierzkowski, Daniel Strauss, Soeren Xu, Hao Landrein, Benoit Hamant, Olivier Smith, Richard S. Johnston, Iain G. Bassel, George W. Cell Syst Article The control of cell position and division act in concert to dictate multicellular organization in tissues and organs. How these processes shape global order and molecular movement across organs is an outstanding problem in biology. Using live 3D imaging and computational analyses, we extracted networks capturing cellular connectivity dynamics across the Arabidopsis shoot apical meristem (SAM) and topologically analyzed the local and global properties of cellular architecture. Locally generated cell division rules lead to the emergence of global tissue-scale organization of the SAM, facilitating robust global communication. Cells that lie upon more shorter paths have an increased propensity to divide, with division plane placement acting to limit the number of shortest paths their daughter cells lie upon. Cell shape heterogeneity and global cellular organization requires KATANIN, providing a multiscale link between cell geometry, mechanical cell-cell interactions, and global tissue order. Cell Press 2019-01-23 /pmc/articles/PMC6345583/ /pubmed/30660611 http://dx.doi.org/10.1016/j.cels.2018.12.009 Text en © 2018 The Authors http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Article
Jackson, Matthew D.B.
Duran-Nebreda, Salva
Kierzkowski, Daniel
Strauss, Soeren
Xu, Hao
Landrein, Benoit
Hamant, Olivier
Smith, Richard S.
Johnston, Iain G.
Bassel, George W.
Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title_full Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title_fullStr Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title_full_unstemmed Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title_short Global Topological Order Emerges through Local Mechanical Control of Cell Divisions in the Arabidopsis Shoot Apical Meristem
title_sort global topological order emerges through local mechanical control of cell divisions in the arabidopsis shoot apical meristem
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6345583/
https://www.ncbi.nlm.nih.gov/pubmed/30660611
http://dx.doi.org/10.1016/j.cels.2018.12.009
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