Molecular insights into the complex mechanics of plant epidermal cell walls

Abstract

Plants have evolved complex nanofibril-based cell walls to meet diverse biological and physical constraints. How strength and extensibility emerge from the nanoscale-to-mesoscale organization of growing cell walls has long been unresolved. We sought to clarify the mechanical roles of cellulose and matrix polysaccharides by developing a coarse-grained model based on polymer physics that recapitulates aspects of assembly and tensile mechanics of epidermal cell walls. Simple noncovalent binding interactions in the model generate bundled cellulose networks resembling that of primary cell walls and possessing stress-dependent elasticity, stiffening, and plasticity beyond a yield threshold. Plasticity originates from fibril-fibril sliding in aligned cellulose networks. This physical model provides quantitative insight into fundamental questions of plant mechanobiology and reveals design principles of biomaterials that combine stiffness with yielding and extensibility.

Identification and Quantification of Glycans in Whole Cells: Architecture of Microalgal Polysaccharides Described by Solid-State Nuclear Magnetic Resonance

“…Actually, in the primary cell walls of plants, the lateral interactions between cellulose microfibrils were found to be determinant to mechanical properties as revealed by coarse-grained molecular dynamics simulation. 125 Since the structure of cellulose is known to differ in algae and higher plants, the structural function of cellulose in the organization of algal cell walls requires further assessment by comparing the cellulose-deficient strain with cellulose-rich species.…”

A Gain-of-Function Mutant of IAA7 Inhibits Stem Elongation by Transcriptional Repression of EXPA5 Genes in Brassica napus

“…The primary cell wall is composed of three distinctive polysaccharides (cellulose, hemicellulose, and pectin) and is usually organized into multilayer nanostructures, especially in the epidermal wall that physically protect and limit growth of leaves and stems [59,60]. In each layer, the cellulose fibrils are arranged in a common direction, forming a reticulated, noncovalent network, but the direction varies between the layers; hemicellulose bind noncovalently to cellulose, and well-hydrated pectins form a gel-like matrix hosting the stiff cellulose network [61]. However, the structure-function of primary plant cell walls is not well understood.…”

“…The latest analysis of cell wall models shows that cellulose noncovalently binds together, providing stress-dependent elasticity, stiffening, and then slide over each other as the cell is stretched, thereby providing plasticity. Thus, cellulose is key to the cell wall's strength, rigidity and plasticity [61]. Expansins were discovered in cell walls from cucumber as they responsible for wall extension [62].…”

Xyloglucan remodelling enzymes and the mechanics of plant seed and fruit biology

“…A machinery of specific glycosyl transferases, transglycosidases, and hydroxylases generates the diversity in XyG structures, with XyG α-1,6-xyosyltransferases (XXTs) adding αXyl residues, and α-xylosidases (αXYLs) cleaving xyloysl residues from the non-reducing end of XyG cell wall components and XyG oligosaccharides ( Frankova et al , 2013 ; Pauly et al , 2016 ; B. Zhang et al , 2021 ). Interestingly, while XyG-deficient A. thaliana xxt mutants exhibit only minor morphological phenotype changes, xyl1 mutants lacking α-xylosidase enzyme activity exhibit altered XyG side chains, free XyG oligosaccharide accumulation, and specific phenotypic defects during reproduction, seed dispersal, germination, and seedling growth.…”

“…XyG oligosaccharides were also proposed to directly or indirectly mediate cell wall signalling which can result in altered hormonal biosynthesis or signalling ( Frankova et al , 2013 ; Pauly et al , 2016 ; Sechet et al , 2016 ; Shigeyama et al , 2016 ; B. Zhang et al , 2021 ). The structure of XyG differs between plant species especially in diversity of the side chains; however, despite this, conservation in XyG remodelling mechanisms and enzymes was also established ( Pauly et al , 2016 ; Rubianes et al , 2019 ; Holloway et al , 2021 ).…”