Molecular insights into the complex mechanics of plant epidermal cell walls.

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.

Nanoscale movements of cellulose microfibrils in primary cell walls.

The growing plant cell wall is commonly considered to be a fibre-reinforced structure whose strength, extensibility and anisotropy depend on the orientation of crystalline cellulose microfibrils, their bonding to the polysaccharide matrix and matrix viscoelasticity1-4. Structural reinforcement of the wall by stiff cellulose microfibrils is central to contemporary models of plant growth, mechanics and meristem dynamics4-12. Although passive microfibril reorientation during wall extension has been inferred from theory and from bulk measurements13-15, nanometre-scale movements of individual microfibrils have not been directly observed. Here we combined nanometre-scale imaging of wet cell walls by atomic force microscopy (AFM) with a stretching device and endoglucanase treatment that induces wall stress relaxation and creep, mimicking wall behaviours during cell growth. Microfibril movements during forced mechanical extensions differ from those during creep of the enzymatically loosened wall. In addition to passive angular reorientation, we observed a diverse repertoire of microfibril movements that reveal the spatial scale of molecular connections between microfibrils. Our results show that wall loosening alters microfibril connectivity, enabling microfibril dynamics not seen during mechanical stretch. These insights into microfibril movements and connectivities need to be incorporated into refined models of plant cell wall structure, growth and morphogenesis.

Class B beta-expansins are needed for pollen separation and stigma penetration.

Group 1 grass pollen allergens comprise a distinctive clade within the beta-expansin family of cell wall-loosening proteins and are divided by sequence divergence into two phylogenetically separable classes (A and B). They have been proposed to loosen the walls of the stigma and style. Supporting this idea, we recently showed that a transposon insertion in one of the maize group-1 allergen genes reduces the ability of pollen to effect fertilization under conditions of pollen competition. In this work, we provide additional information on the phenotype of this mutant, showing that pollen deficient in beta-expansin gene expression tended to form large aggregates, leading to poor pollen dispersal on anther dehiscence, and that emerging pollen tubes had difficulties entering the silk. In addition, a silencing construct was created to reduce expression of all the class B genes with results that are consistent with those seen with the transposon insertional line, including reduced transgene transmission through the pollen. Our results provide a more detailed understanding of the role of group 1 allergens (pollen beta-expansins) in maize pollen development, pollen dispersal, pollen tube penetration into the style, and pollen tube growth through the transmitting tract.