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A computational framework for cortical microtubule dynamics in realistically shaped plant cells

Plant morphogenesis is strongly dependent on the directional growth and the subsequent oriented division of individual cells. It has been shown that the plant cortical microtubule array plays a key role in controlling both these processes. This ordered structure emerges as the collective result of s...

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Autores principales: Chakrabortty, Bandan, Blilou, Ikram, Scheres, Ben, Mulder, Bela M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5812663/
https://www.ncbi.nlm.nih.gov/pubmed/29394250
http://dx.doi.org/10.1371/journal.pcbi.1005959
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author Chakrabortty, Bandan
Blilou, Ikram
Scheres, Ben
Mulder, Bela M.
author_facet Chakrabortty, Bandan
Blilou, Ikram
Scheres, Ben
Mulder, Bela M.
author_sort Chakrabortty, Bandan
collection PubMed
description Plant morphogenesis is strongly dependent on the directional growth and the subsequent oriented division of individual cells. It has been shown that the plant cortical microtubule array plays a key role in controlling both these processes. This ordered structure emerges as the collective result of stochastic interactions between large numbers of dynamic microtubules. To elucidate this complex self-organization process a number of analytical and computational approaches to study the dynamics of cortical microtubules have been proposed. To date, however, these models have been restricted to two dimensional planes or geometrically simple surfaces in three dimensions, which strongly limits their applicability as plant cells display a wide variety of shapes. This limitation is even more acute, as both local as well as global geometrical features of cells are expected to influence the overall organization of the array. Here we describe a framework for efficiently simulating microtubule dynamics on triangulated approximations of arbitrary three dimensional surfaces. This allows the study of microtubule array organization on realistic cell surfaces obtained by segmentation of microscopic images. We validate the framework against expected or known results for the spherical and cubical geometry. We then use it to systematically study the individual contributions of global geometry, cell-edge induced catastrophes and cell-face induced stability to array organization in a cuboidal geometry. Finally, we apply our framework to analyze the highly non-trivial geometry of leaf pavement cells of Arabidopsis thaliana, Nicotiana benthamiana and Hedera helix. We show that our simulations can predict multiple features of the microtubule array structure in these cells, revealing, among others, strong constraints on the orientation of division planes.
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spelling pubmed-58126632018-02-28 A computational framework for cortical microtubule dynamics in realistically shaped plant cells Chakrabortty, Bandan Blilou, Ikram Scheres, Ben Mulder, Bela M. PLoS Comput Biol Research Article Plant morphogenesis is strongly dependent on the directional growth and the subsequent oriented division of individual cells. It has been shown that the plant cortical microtubule array plays a key role in controlling both these processes. This ordered structure emerges as the collective result of stochastic interactions between large numbers of dynamic microtubules. To elucidate this complex self-organization process a number of analytical and computational approaches to study the dynamics of cortical microtubules have been proposed. To date, however, these models have been restricted to two dimensional planes or geometrically simple surfaces in three dimensions, which strongly limits their applicability as plant cells display a wide variety of shapes. This limitation is even more acute, as both local as well as global geometrical features of cells are expected to influence the overall organization of the array. Here we describe a framework for efficiently simulating microtubule dynamics on triangulated approximations of arbitrary three dimensional surfaces. This allows the study of microtubule array organization on realistic cell surfaces obtained by segmentation of microscopic images. We validate the framework against expected or known results for the spherical and cubical geometry. We then use it to systematically study the individual contributions of global geometry, cell-edge induced catastrophes and cell-face induced stability to array organization in a cuboidal geometry. Finally, we apply our framework to analyze the highly non-trivial geometry of leaf pavement cells of Arabidopsis thaliana, Nicotiana benthamiana and Hedera helix. We show that our simulations can predict multiple features of the microtubule array structure in these cells, revealing, among others, strong constraints on the orientation of division planes. Public Library of Science 2018-02-02 /pmc/articles/PMC5812663/ /pubmed/29394250 http://dx.doi.org/10.1371/journal.pcbi.1005959 Text en © 2018 Chakrabortty et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Chakrabortty, Bandan
Blilou, Ikram
Scheres, Ben
Mulder, Bela M.
A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title_full A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title_fullStr A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title_full_unstemmed A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title_short A computational framework for cortical microtubule dynamics in realistically shaped plant cells
title_sort computational framework for cortical microtubule dynamics in realistically shaped plant cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5812663/
https://www.ncbi.nlm.nih.gov/pubmed/29394250
http://dx.doi.org/10.1371/journal.pcbi.1005959
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