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Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach

BACKGROUND: Morphological properties of tissues and organs rely on cell growth. The growth of plant cells is determined by properties of a tough outer cell wall that deforms anisotropically in response to high turgor pressure. Cortical microtubules bias the mechanical anisotropy of a cell wall by af...

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Autores principales: Li, Jing, Szymanski, Daniel B., Kim, Taeyoon
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10251582/
https://www.ncbi.nlm.nih.gov/pubmed/37291489
http://dx.doi.org/10.1186/s12870-023-04252-5
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author Li, Jing
Szymanski, Daniel B.
Kim, Taeyoon
author_facet Li, Jing
Szymanski, Daniel B.
Kim, Taeyoon
author_sort Li, Jing
collection PubMed
description BACKGROUND: Morphological properties of tissues and organs rely on cell growth. The growth of plant cells is determined by properties of a tough outer cell wall that deforms anisotropically in response to high turgor pressure. Cortical microtubules bias the mechanical anisotropy of a cell wall by affecting the trajectories of cellulose synthases in the wall that polymerize cellulose microfibrils. The microtubule cytoskeleton is often oriented in one direction at cellular length-scales to regulate growth direction, but the means by which cellular-scale microtubule patterns emerge has not been well understood. Correlations between the microtubule orientation and tensile forces in the cell wall have often been observed. However, the plausibility of stress as a determining factor for microtubule patterning has not been directly evaluated to date. RESULTS: Here, we simulated how different attributes of tensile forces in the cell wall can orient and pattern the microtubule array in the cortex. We implemented a discrete model with transient microtubule behaviors influenced by local mechanical stress in order to probe the mechanisms of stress-dependent patterning. Specifically, we varied the sensitivity of four types of dynamic behaviors observed on the plus end of microtubules – growth, shrinkage, catastrophe, and rescue – to local stress. Then, we evaluated the extent and rate of microtubule alignments in a two-dimensional computational domain that reflects the structural organization of the cortical array in plant cells. CONCLUSION: Our modeling approaches reproduced microtubule patterns observed in simple cell types and demonstrated that a spatial variation in the magnitude and anisotropy of stress can mediate mechanical feedback between the wall and of the cortical microtubule array. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04252-5.
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spelling pubmed-102515822023-06-10 Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach Li, Jing Szymanski, Daniel B. Kim, Taeyoon BMC Plant Biol Research BACKGROUND: Morphological properties of tissues and organs rely on cell growth. The growth of plant cells is determined by properties of a tough outer cell wall that deforms anisotropically in response to high turgor pressure. Cortical microtubules bias the mechanical anisotropy of a cell wall by affecting the trajectories of cellulose synthases in the wall that polymerize cellulose microfibrils. The microtubule cytoskeleton is often oriented in one direction at cellular length-scales to regulate growth direction, but the means by which cellular-scale microtubule patterns emerge has not been well understood. Correlations between the microtubule orientation and tensile forces in the cell wall have often been observed. However, the plausibility of stress as a determining factor for microtubule patterning has not been directly evaluated to date. RESULTS: Here, we simulated how different attributes of tensile forces in the cell wall can orient and pattern the microtubule array in the cortex. We implemented a discrete model with transient microtubule behaviors influenced by local mechanical stress in order to probe the mechanisms of stress-dependent patterning. Specifically, we varied the sensitivity of four types of dynamic behaviors observed on the plus end of microtubules – growth, shrinkage, catastrophe, and rescue – to local stress. Then, we evaluated the extent and rate of microtubule alignments in a two-dimensional computational domain that reflects the structural organization of the cortical array in plant cells. CONCLUSION: Our modeling approaches reproduced microtubule patterns observed in simple cell types and demonstrated that a spatial variation in the magnitude and anisotropy of stress can mediate mechanical feedback between the wall and of the cortical microtubule array. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04252-5. BioMed Central 2023-06-09 /pmc/articles/PMC10251582/ /pubmed/37291489 http://dx.doi.org/10.1186/s12870-023-04252-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Li, Jing
Szymanski, Daniel B.
Kim, Taeyoon
Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title_full Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title_fullStr Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title_full_unstemmed Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title_short Probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
title_sort probing stress-regulated ordering of the plant cortical microtubule array via a computational approach
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10251582/
https://www.ncbi.nlm.nih.gov/pubmed/37291489
http://dx.doi.org/10.1186/s12870-023-04252-5
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