Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants

Mechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense...

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Main Authors: Antoine Fruleux, Stéphane Verger, Arezki Boudaoud
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00757/full
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author Antoine Fruleux
Stéphane Verger
Arezki Boudaoud
author_facet Antoine Fruleux
Stéphane Verger
Arezki Boudaoud
author_sort Antoine Fruleux
collection DOAJ
description Mechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense and how this would occur. Here we briefly explain the notions of mechanical stress and strain. We present the challenges to understand their sensing by plants, focusing on the cell wall and the plasma membrane, and we review putative mechanosensing structures. We propose minimal biophysical models of mechanosensing, revealing the modes of mechanosensing according to mechanosensor lifetime, threshold force for mechanosensor dissociation, and type of association between the mechanosensor and the cell wall, as the sensor may be associated to a major load-bearing structure such as cellulose or to a minor load-bearing structure such as pectins or the plasma membrane. Permanent strain, permanent expansion, and relatively slow variations thereof are sensed in all cases; variations of stress are sensed in all cases; permanent stress is sensed only in the following specific cases: sensors associated to minor load-bearing structures slowly relaxing in a growing wall, long-lived sensors with high dissociation force and associated to major-load-bearing structures, and sensors with low dissociation force associated to major-load-baring structures behaving elastically. We also find that all sensors respond to variations in the composition or the mechanical properties of the cell wall. The level of sensing is modulated by the properties of all of mechanosensor, cell wall components, and plasma membrane. Although our models are minimal and not fully realistic, our results yield a framework to start investigating the possible functions of putative mechanosensors.
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spelling doaj.art-1a26eac7dabd46f7a3010bd3edefb3b52022-12-22T02:04:34ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-06-011010.3389/fpls.2019.00757454676Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in PlantsAntoine Fruleux0Stéphane Verger1Arezki Boudaoud2Laboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, Lyon, FranceDepartment of Forest Genetics and Plant Physiology, Umeå Plant Science Centre, Swedish University of Agricultural Sciences, Umeå, SwedenLaboratoire de Reproduction et Développement des Plantes, Université de Lyon, ENS de Lyon, UCBL, INRA, CNRS, Lyon, FranceMechanical signals have recently emerged as a major cue in plant morphogenesis, notably influencing cytoskeleton organization, gene expression, protein polarity, or cell division. Although many putative mechanosensing proteins have been identified, it is unclear what mechanical cue they might sense and how this would occur. Here we briefly explain the notions of mechanical stress and strain. We present the challenges to understand their sensing by plants, focusing on the cell wall and the plasma membrane, and we review putative mechanosensing structures. We propose minimal biophysical models of mechanosensing, revealing the modes of mechanosensing according to mechanosensor lifetime, threshold force for mechanosensor dissociation, and type of association between the mechanosensor and the cell wall, as the sensor may be associated to a major load-bearing structure such as cellulose or to a minor load-bearing structure such as pectins or the plasma membrane. Permanent strain, permanent expansion, and relatively slow variations thereof are sensed in all cases; variations of stress are sensed in all cases; permanent stress is sensed only in the following specific cases: sensors associated to minor load-bearing structures slowly relaxing in a growing wall, long-lived sensors with high dissociation force and associated to major-load-bearing structures, and sensors with low dissociation force associated to major-load-baring structures behaving elastically. We also find that all sensors respond to variations in the composition or the mechanical properties of the cell wall. The level of sensing is modulated by the properties of all of mechanosensor, cell wall components, and plasma membrane. Although our models are minimal and not fully realistic, our results yield a framework to start investigating the possible functions of putative mechanosensors.https://www.frontiersin.org/article/10.3389/fpls.2019.00757/fullmechanosensingmechanical signalstressstraincell wallbiophysical model
spellingShingle Antoine Fruleux
Stéphane Verger
Arezki Boudaoud
Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
Frontiers in Plant Science
mechanosensing
mechanical signal
stress
strain
cell wall
biophysical model
title Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
title_full Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
title_fullStr Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
title_full_unstemmed Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
title_short Feeling Stressed or Strained? A Biophysical Model for Cell Wall Mechanosensing in Plants
title_sort feeling stressed or strained a biophysical model for cell wall mechanosensing in plants
topic mechanosensing
mechanical signal
stress
strain
cell wall
biophysical model
url https://www.frontiersin.org/article/10.3389/fpls.2019.00757/full
work_keys_str_mv AT antoinefruleux feelingstressedorstrainedabiophysicalmodelforcellwallmechanosensinginplants
AT stephaneverger feelingstressedorstrainedabiophysicalmodelforcellwallmechanosensinginplants
AT arezkiboudaoud feelingstressedorstrainedabiophysicalmodelforcellwallmechanosensinginplants