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      Mechanical factors contributing to the Venus flytrap’s rate-dependent response to stimuli

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          Abstract

          The sensory hairs of the Venus flytrap ( Dionaea muscipula Ellis) detect mechanical stimuli imparted by their prey and fire bursts of electrical signals called action potentials (APs). APs are elicited when the hairs are sufficiently stimulated and two consecutive APs can trigger closure of the trap. Earlier experiments have identified thresholds for the relevant stimulus parameters, namely the angular displacement \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\theta $$\end{document} and angular velocity \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\omega $$\end{document} . However, these experiments could not trace the deformation of the trigger hair’s sensory cells, which are known to transduce the mechanical stimulus. To understand the kinematics at the cellular level, we investigate the role of two relevant mechanical phenomena: viscoelasticity and intercellular fluid transport using a multi-scale numerical model of the sensory hair. We hypothesize that the combined influence of these two phenomena and \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\omega $$\end{document} contribute to the flytrap’s rate-dependent response to stimuli. In this study, we firstly perform sustained deflection tests on the hair to estimate the viscoelastic material properties of the tissue. Thereafter, through simulations of hair deflection tests at different loading rates, we were able to establish a multi-scale kinematic link between \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\omega $$\end{document} and the cell wall stretch \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\delta $$\end{document} . Furthermore, we find that the rate at which \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\delta $$\end{document} evolves during a stimulus is also proportional to \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\omega $$\end{document} . This suggests that mechanosensitive ion channels, expected to be stretch-activated and localized in the plasma membrane of the sensory cells, could be additionally sensitive to the rate at which stretch is applied.

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          Most cited references 28

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          Ion channels in plants.

          Since the first recordings of single potassium channel activities in the plasma membrane of guard cells more than 25 years ago, patch-clamp studies discovered a variety of ion channels in all cell types and plant species under inspection. Their properties differed in a cell type- and cell membrane-dependent manner. Guard cells, for which the existence of plant potassium channels was initially documented, advanced to a versatile model system for studying plant ion channel structure, function, and physiology. Interestingly, one of the first identified potassium-channel genes encoding the Shaker-type channel KAT1 was shown to be highly expressed in guard cells. KAT1-type channels from Arabidopsis thaliana and its homologs from other species were found to encode the K(+)-selective inward rectifiers that had already been recorded in early patch-clamp studies with guard cells. Within the genome era, additional Arabidopsis Shaker-type channels appeared. All nine members of the Arabidopsis Shaker family are localized at the plasma membrane, where they either operate as inward rectifiers, outward rectifiers, weak voltage-dependent channels, or electrically silent, but modulatory subunits. The vacuole membrane, in contrast, harbors a set of two-pore K(+) channels. Just very recently, two plant anion channel families of the SLAC/SLAH and ALMT/QUAC type were identified. SLAC1/SLAH3 and QUAC1 are expressed in guard cells and mediate Slow- and Rapid-type anion currents, respectively, that are involved in volume and turgor regulation. Anion channels in guard cells and other plant cells are key targets within often complex signaling networks. Here, the present knowledge is reviewed for the plant ion channel biology. Special emphasis is drawn to the molecular mechanisms of channel regulation, in the context of model systems and in the light of evolution.
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            Stretch-activated ion channels: what are they?

            Mechanosensitive ion channels (MSCs) exist in all cells, but mechanosensitivity is a phenotype not a genotype. Specialized mechanoreceptors such as the hair cells of the cochlea require elaborate mechanical impedance matching to couple the channels to the external stress. In contrast, MSCs in nonspecialized cells appear activated by stress in the bilayer local to the channel--within about three lipids. Local mechanical stress can be produced by far-field tension, amphipaths, phase separations, the cytoskeleton, the extracellular matrix, and the adhesion energy between the membrane and a patch pipette. Understanding MSC function requires under standing the stimulus.
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              Mechanosensitive channels: what can they do and how do they do it?

              While mechanobiological processes employ diverse mechanisms, at their heart are force-induced perturbations in the structure and dynamics of molecules capable of triggering subsequent events. Among the best characterized force-sensing systems are bacterial mechanosensitive channels. These channels reflect an intimate coupling of protein conformation with the mechanics of the surrounding membrane; the membrane serves as an adaptable sensor that responds to an input of applied force and converts it into an output signal, interpreted for the cell by mechanosensitive channels. The cell can exploit this information in a number of ways: ensuring cellular viability in the presence of osmotic stress and perhaps also serving as a signal transducer for membrane tension or other functions. This review focuses on the bacterial mechanosensitive channels of large (MscL) and small (MscS) conductance and their eukaryotic homologs, with an emphasis on the outstanding issues surrounding the function and mechanism of this fascinating class of molecules. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                esaikia@ethz.ch
                fwittel@ethz.ch
                Journal
                Biomech Model Mechanobiol
                Biomech Model Mechanobiol
                Biomechanics and Modeling in Mechanobiology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1617-7959
                1617-7940
                24 August 2021
                24 August 2021
                2021
                : 20
                : 6
                : 2287-2297
                Affiliations
                [1 ]GRID grid.5801.c, ISNI 0000 0001 2156 2780, Department of Civil, Environmental and Geomatic Engineering, , ETH Zurich, ; Zurich, 8093 Switzerland
                [2 ]GRID grid.5801.c, ISNI 0000 0001 2156 2780, Department of Mechanical and Process Engineering, , ETH Zurich, ; Zurich, 8092 Switzerland
                [3 ]GRID grid.7400.3, ISNI 0000 0004 1937 0650, Department of Plant and Microbial Biology and Zurich-Basel Plant Science Center, , University of Zurich, ; Zurich, 8008 Switzerland
                [4 ]GRID grid.506541.3, ISNI 0000 0004 0426 6279, Institut für Holztechnologie, ; 01217 Dresden, Germany
                [5 ]GRID grid.464131.5, ISNI 0000 0004 0370 1507, Laboratoire de Physique et Mécanique des Milieux Hétérogènes, École Supérieur de Physique et de Chimie Industrielles de la Ville de Paris, ; 75005 Paris, France
                [6 ]GRID grid.7354.5, ISNI 0000 0001 2331 3059, Swiss Federal Laboratories for Material Science and Technology-EMPA, Cellulose and Wood Materials Laboratory, ; 8600 Dubendorf, Switzerland
                [7 ]GRID grid.5335.0, ISNI 0000000121885934, Department of Chemical Engineering and Biotechnology, , University of Cambridge, ; Cambridge, CB3 0AS United Kingdom
                Article
                1507
                10.1007/s10237-021-01507-8
                8595191
                34431032
                6915c1bb-4b04-4504-af9e-e436cda94415
                © The Author(s) 2021, corrected publication, 2021

                Open AccessThis 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/.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, schweizerischer nationalfonds zur förderung der wissenschaftlichen forschung;
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, schweizerischer nationalfonds zur förderung der wissenschaftlichen forschung;
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, schweizerischer nationalfonds zur förderung der wissenschaftlichen forschung;
                Award ID: CR22I2 166110
                Award Recipient :
                Funded by: ETH Zurich
                Categories
                Original Paper
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                © Springer-Verlag GmbH Germany, part of Springer Nature 2021

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