Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum

Studies on the mechanics of plant cells usually focus on understanding the effects of turgor pressure and properties of the cell wall (CW). While the functional roles of the underlying cytoskeleton have been studied, the extent to which it contributes to the mechanical properties of cells is not elu...

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Main Authors: Leah Ginsberg, Robin McDonald, Qinchen Lin, Rodinde Hendrickx, Giada Spigolon, Guruswami Ravichandran, Chiara Daraio, Eleftheria Roumeli
Format: Article
Language:English
Published: Cambridge University Press 2022-01-01
Series:Quantitative Plant Biology
Subjects:
Online Access:https://www.cambridge.org/core/product/identifier/S2632882821000151/type/journal_article
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author Leah Ginsberg
Robin McDonald
Qinchen Lin
Rodinde Hendrickx
Giada Spigolon
Guruswami Ravichandran
Chiara Daraio
Eleftheria Roumeli
author_facet Leah Ginsberg
Robin McDonald
Qinchen Lin
Rodinde Hendrickx
Giada Spigolon
Guruswami Ravichandran
Chiara Daraio
Eleftheria Roumeli
author_sort Leah Ginsberg
collection DOAJ
description Studies on the mechanics of plant cells usually focus on understanding the effects of turgor pressure and properties of the cell wall (CW). While the functional roles of the underlying cytoskeleton have been studied, the extent to which it contributes to the mechanical properties of cells is not elucidated. Here, we study the contributions of the CW, microtubules (MTs) and actin filaments (AFs), in the mechanical properties of Nicotiana tabacum cells. We use a multiscale biomechanical assay comprised of atomic force microscopy and micro-indentation in solutions that (i) remove MTs and AFs and (ii) alter osmotic pressures in the cells. To compare measurements obtained by the two mechanical tests, we develop two generative statistical models to describe the cell’s behaviour using one or both datasets. Our results illustrate that MTs and AFs contribute significantly to cell stiffness and dissipated energy, while confirming the dominant role of turgor pressure.
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spelling doaj.art-72a90f31f33246c188a943ca1f92b05f2023-03-09T12:43:35ZengCambridge University PressQuantitative Plant Biology2632-88282022-01-01310.1017/qpb.2021.15Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacumLeah Ginsberg0Robin McDonald1Qinchen Lin2Rodinde Hendrickx3Giada Spigolon4Guruswami Ravichandran5Chiara Daraio6Eleftheria Roumeli7https://orcid.org/0000-0002-2828-1428Division of Engineering and Applied Science, California Institute of Technology, Pasadena, CA 91125, USADivision of Engineering and Applied Science, California Institute of Technology, Pasadena, CA 91125, USADepartment of Materials Science and Engineering, University of Washington, Seattle, WA 98195, USADivision of Engineering and Applied Science, California Institute of Technology, Pasadena, CA 91125, USABiological Imaging Facility, California Institute of Technology, Pasadena, CA 91125, USADivision of Engineering and Applied Science, California Institute of Technology, Pasadena, CA 91125, USADivision of Engineering and Applied Science, California Institute of Technology, Pasadena, CA 91125, USADepartment of Materials Science and Engineering, University of Washington, Seattle, WA 98195, USAStudies on the mechanics of plant cells usually focus on understanding the effects of turgor pressure and properties of the cell wall (CW). While the functional roles of the underlying cytoskeleton have been studied, the extent to which it contributes to the mechanical properties of cells is not elucidated. Here, we study the contributions of the CW, microtubules (MTs) and actin filaments (AFs), in the mechanical properties of Nicotiana tabacum cells. We use a multiscale biomechanical assay comprised of atomic force microscopy and micro-indentation in solutions that (i) remove MTs and AFs and (ii) alter osmotic pressures in the cells. To compare measurements obtained by the two mechanical tests, we develop two generative statistical models to describe the cell’s behaviour using one or both datasets. Our results illustrate that MTs and AFs contribute significantly to cell stiffness and dissipated energy, while confirming the dominant role of turgor pressure.https://www.cambridge.org/core/product/identifier/S2632882821000151/type/journal_articlecell wallcytoskeletonmicro-indentationnano-indentation Nicotiana tabacum statistical modeling
spellingShingle Leah Ginsberg
Robin McDonald
Qinchen Lin
Rodinde Hendrickx
Giada Spigolon
Guruswami Ravichandran
Chiara Daraio
Eleftheria Roumeli
Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
Quantitative Plant Biology
cell wall
cytoskeleton
micro-indentation
nano-indentation
Nicotiana tabacum
statistical modeling
title Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
title_full Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
title_fullStr Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
title_full_unstemmed Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
title_short Cell wall and cytoskeletal contributions in single cell biomechanics of Nicotiana tabacum
title_sort cell wall and cytoskeletal contributions in single cell biomechanics of nicotiana tabacum
topic cell wall
cytoskeleton
micro-indentation
nano-indentation
Nicotiana tabacum
statistical modeling
url https://www.cambridge.org/core/product/identifier/S2632882821000151/type/journal_article
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