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Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules

Although microtubules in plant cells have been extensively studied, the mechanisms that regulate the spatial organization of microtubules are poorly understood. We hypothesize that the interaction between microtubules and cytoplasmic flow plays an important role in the assembly and orientation of mi...

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Autores principales: Murshed, Mohammad, Wei, Donghui, Gu, Ying, Wang, Jin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10368657/
https://www.ncbi.nlm.nih.gov/pubmed/37502315
http://dx.doi.org/10.1002/pld3.505
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author Murshed, Mohammad
Wei, Donghui
Gu, Ying
Wang, Jin
author_facet Murshed, Mohammad
Wei, Donghui
Gu, Ying
Wang, Jin
author_sort Murshed, Mohammad
collection PubMed
description Although microtubules in plant cells have been extensively studied, the mechanisms that regulate the spatial organization of microtubules are poorly understood. We hypothesize that the interaction between microtubules and cytoplasmic flow plays an important role in the assembly and orientation of microtubules. To test this hypothesis, we developed a new computational modeling framework for microtubules based on theory and methods from the fluid–structure interaction. We employed the immersed boundary method to track the movement of microtubules in cytoplasmic flow. We also incorporated details of the encounter dynamics when two microtubules collide with each other. We verified our computational model through several numerical tests before applying it to the simulation of the microtubule–cytoplasm interaction in a growing plant cell. Our computational investigation demonstrated that microtubules are primarily oriented in the direction orthogonal to the axis of cell elongation. We validated the simulation results through a comparison with the measurement from laboratory experiments. We found that our computational model, with further calibration, was capable of generating microtubule orientation patterns that were qualitatively and quantitatively consistent with the experimental results. The computational model proposed in this study can be naturally extended to many other cellular systems that involve the interaction between microstructures and the intracellular fluid.
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spelling pubmed-103686572023-07-27 Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules Murshed, Mohammad Wei, Donghui Gu, Ying Wang, Jin Plant Direct Research Articles Although microtubules in plant cells have been extensively studied, the mechanisms that regulate the spatial organization of microtubules are poorly understood. We hypothesize that the interaction between microtubules and cytoplasmic flow plays an important role in the assembly and orientation of microtubules. To test this hypothesis, we developed a new computational modeling framework for microtubules based on theory and methods from the fluid–structure interaction. We employed the immersed boundary method to track the movement of microtubules in cytoplasmic flow. We also incorporated details of the encounter dynamics when two microtubules collide with each other. We verified our computational model through several numerical tests before applying it to the simulation of the microtubule–cytoplasm interaction in a growing plant cell. Our computational investigation demonstrated that microtubules are primarily oriented in the direction orthogonal to the axis of cell elongation. We validated the simulation results through a comparison with the measurement from laboratory experiments. We found that our computational model, with further calibration, was capable of generating microtubule orientation patterns that were qualitatively and quantitatively consistent with the experimental results. The computational model proposed in this study can be naturally extended to many other cellular systems that involve the interaction between microstructures and the intracellular fluid. John Wiley and Sons Inc. 2023-07-25 /pmc/articles/PMC10368657/ /pubmed/37502315 http://dx.doi.org/10.1002/pld3.505 Text en © 2023 The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.
spellingShingle Research Articles
Murshed, Mohammad
Wei, Donghui
Gu, Ying
Wang, Jin
Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title_full Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title_fullStr Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title_full_unstemmed Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title_short Simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
title_sort simulation of microtubule–cytoplasm interaction revealed the importance of fluid dynamics in determining the organization of microtubules
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10368657/
https://www.ncbi.nlm.nih.gov/pubmed/37502315
http://dx.doi.org/10.1002/pld3.505
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