Regulation of plant cell wall stiffness by mechanical stress: a mesoscale physical model

Abstract

A crucial question in developmental biology is how cell growth is coordinated in living tissue to generate complex and reproducible shapes. We address this issue here in plants, where stiff extracellular walls prevent cell migration and morphogenesis mostly results from growth driven by turgor pressure. How cells grow in response to pressure partly depends on the mechanical properties of their walls, which are generally heterogeneous, anisotropic and dynamic. The active control of these properties is therefore a cornerstone of plant morphogenesis.Here, we focus on wall stiffness, which is under the control of both molecular and mechanical signaling. Indeed, in plant tissues, the balance between turgor and cell wall elasticity generates a tissue-wide stress field. Within cells, mechanosensitive structures, such as cortical microtubules, adapt their behavior accordingly and locally influence cell wall remodeling dynamics. To fully apprehend the properties of this feedback loop, modeling approaches are indispensable. To that end, several modeling tools in the form of virtual tissues have been developed. However, these models often relate mechanical stress and cell wall stiffness in relatively abstract manners, where the molecular specificities of the various actors are not fully captured.In this paper, we propose to refine this approach by including parsimonious biochemical and biomechanical properties of the main molecular actors involved. Through a coarse-grained approach and through finite element simulations, we study the role of stress-sensing microtubules on organ-scale mechanics.

Disentangling loosening from softening: insights into primary cell wall structure

“…We note that in this study xyloglucanase (XEG) treatment did not impact any of the biomechanical measures, but did have effects when combined with cellulase activity, extending results obtained in a previous study with other cell walls (Park and Cosgrove, 2012b). Recent simulations of cell wall growth based on elastic deformations of finite element models (Yanagisawa et al ., ; Majda et al ., ; Bidhendi and Geitmann, ; Sapala et al ., ; Oliveri et al ., ) assume the wall is faithfully represented as a simple fiber‐reinforced elastic hydrogel, but such a material lacks many of the material properties reported here. Results in this study, along with previous work on the same material (Kim et al ., ; Zamil et al ., ; Zhang et al ., , ), provide key data for development of more realistic molecular models to connect cell wall structure with wall mechanics and to elucidate the molecular basis of wall‐loosening processes underlying cell growth.…”

“…The tethering concept is challenged by the results of studies where xyloglucan was removed genetically (Cavalier et al ., ; Park and Cosgrove, 2012a) or enzymatically (Park and Cosgrove, 2012b) as well as by AFM‐based imaging of microfibril movements in extending primary cell walls (Zhang et al ., ). It also contrasts with concepts of the primary cell wall as a simple fiber‐reinforced hydrogel, in which cellulose microfibrils function primarily as stiff rods that mechanically reinforce a gel‐like viscoelastic matrix (Probine and Barber, ; Preston, ; Taiz, ; Milani et al ., ; Oliveri et al ., ). Under the latter concept, wall enlargement is based on viscoelasticity of the matrix.…”

Simulating Turgor-Induced Stress Patterns in Multilayered Plant Tissues

“…Consequently, a common strategy in most of the existing modeling approaches is to restrict the influence of inner tissues to pressure forces applied onto the epidermis and to focus only on the mechanics of this outermost layer described as a pressure vessel. Such approaches either described the epidermis as a two-dimensional (2D) curved continuum (Hamant et al 2008;Bozorg et al 2014;Oliveri et al 2018;Kierzkowski et al 2012) or as a single layer of cells fixed on a flat surface (Sampathkumar et al 2014;Sapala et al 2018).…”

Multiscale mechanical model for cell division orientation in developing biological systems

“…Thanks to the burst of new technologies and the consequent availability of quantitative morphodynamic data [4][5][6][7], the dynamics of shapes and its robustness against environmental and intrinsic noise is being investigated under a new paradigm, in which the shape itself drives its own change by feeding back on its own functioning. Several works have shown different aspects of this general idea [8][9][10][11][12][13][14][15][16]. One important process known to be driven by cell shape is cell division.…”