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

Abstract

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.

Mechanical feedback-loop regulation of morphogenesis in plants

“…Recently, microtubules themselves have been proposed to play the role of tension sensors in plants (Hamant et al, 2019), based on the observation that physical confinement of relatively stiff microtubules to a specific threedimensional space results in the emergence of certain patterns (Mirabet et al, 2018). However, the presence of a cell wall-plasma membrane-microtubule continuum is more compelling (Hamant et al, 2019), because the transduction of mechanical forces requires the presence of a solid medium that has a network-like property to ensure transmission of mechanical forces over a specific distance (Hamant et al, 2019;Fruleux et al, 2019). As discussed above, the pre-tensed CMFs are organized as lamellate sheets and form an interconnected network-like structure; thus, CMFs serve as ideal candidates for transmitting such mechanical signals (Cosgrove, 2018b) (Fig.…”

“…Recent advances in plant mechanobiology have started to reveal the role of plasma membrane-localized proteins involved in mechanosensing (Fruleux et al, 2019) The transmission of mechanical forces at the plane of the plasma membrane is much simpler than the complex three dimensional network of the cell wall. Therefore, there are direct consequences of structural modifications of these proteins present at the plasma membrane.…”

Extracellular matrix and wall composition are diverse in the organogenic and non-organogenic calli of Actinidia arguta

“…This phenomenon relates to hydrated pectins, which are a main component of the primary cell wall (Muscariello et al 2005;Pathan et al 2008;Bidhendi and Geitmann 2016;Broxterman and Schols 2018). Additionally, it is possible that proteins such as extensins, which may be covalently linked with the wall polysaccharides (Fruleux et al 2019 and references therein), affect the organisation of the pectins and finally have an influence on the appearance after CPD treatment. A different appearance of the external layer in the SEM analyses, which was dependent on the SEM procedure, was described earlier (Popielarska-Konieczna et al 2010).…”

Charged pore-lining residues are required for normal channel kinetics in the eukaryotic mechanosensitive ion channel MSL1

“…Living organisms constantly experience physical force from both internal and external sources and possess a variety of mechanisms for detecting and responding to key mechanical stimuli [1][2][3]. Among these mechanisms are mechanosensitive (MS) ion channels, which are found in all kingdoms of life [4][5][6][7].…”