Gradients in Wall Mechanics and Polysaccharides along Growing Inflorescence Stems

Abstract

At early stages of Arabidopsis (Arabidopsis thaliana) flowering, the inflorescence stem undergoes rapid growth, with elongation occurring predominantly in the apical ;4 cm of the stem. We measured the spatial gradients for elongation rate, osmotic pressure, cell wall thickness, and wall mechanical compliances and coupled these macroscopic measurements with molecular-level characterization of the polysaccharide composition, mobility, hydration, and intermolecular interactions of the inflorescence cell wall using solid-state nuclear magnetic resonance spectroscopy and small-angle neutron scattering. Force-extension curves revealed a gradient, from high to low, in the plastic and elastic compliances of cell walls along the elongation zone, but plots of growth rate versus wall compliances were strikingly nonlinear. Neutron-scattering curves showed only subtle changes in wall structure, including a slight increase in cellulose microfibril alignment along the growing stem. In contrast, solid-state nuclear magnetic resonance spectra showed substantial decreases in pectin amount, esterification, branching, hydration, and mobility in an apical-to-basal pattern, while the cellulose content increased modestly. These results suggest that pectin structural changes are connected with increases in pectin-cellulose interaction and reductions in wall compliances along the apical-to-basal gradient in growth rate. These pectin structural changes may lessen the ability of the cell wall to undergo stress relaxation and irreversible expansion (e.g. induced by expansins), thus contributing to the growth kinematics of the growing stem.

Diffuse Growth of Plant Cell Walls

“…This is surprising because such interactions are not observed in binding studies in vitro (Zykwinska et al, 2008a(Zykwinska et al, , 2008b. A recent study of cell wall properties along the axial growth gradient of the Arabidopsis stem gives additional clues (Phyo et al, 2017). Pectins in the apical (faster-growing and softer) region of the stem are more mobile, more hydrated, more esterified, and more branched compared with pectins in the lower (more slowly growing and stiffer) region of the stem.…”

“…For instance, in the hemispherical tip of growing pollen tubes, de-esterified homogalacturonan is associated with stiffer walls and cessation of wall expansion (Geitmann and Parre, 2004;Sanati Nezhad et al, 2014). Likewise, pectin de-esterification is associated with the decline in the growth rate and increased wall stiffness along the apical-to-basal gradient of growing stems (Goldberg et al, 1986;Phyo et al, 2017). Moreover, wall loosening by expansin is hindered in the basal regions of growing stems where the extent of de-esterified pectin is high (Cosgrove, 1996), and this hindrance may be partially reversed by removal of pectins and calcium (Zhao et al, 2008).…”

Pectin methylesterase selectively softens the onion epidermal wall yet reduces acid-induced creep

“…Other physical mechanisms may contribute to the reduced plasticity: approximately half of the calcium effect may due to electrostatic shielding, judging from the effect of MgCl 2 (Fig. 4) and assuming that Mg 2+ does not form HG crosslinks (Thibault and Rinaudo, 1986); calcium-HG interactions may also reduce HG-cellulose interactions (Lopez-Sanchez et al , 2020; Phyo et al , 2017; Wang et al , 2015). Such interactions may be extensive, but their significance for wall mechanics is uncertain.…”

Plant and algal structure: from cell walls to biomechanical function

“…Pectins have numerous and diverse functions, including cell wall hydration, support, defence and storage. However, pectins also interact with cellulose microfibrils, either through binding of pectin side chains to cellulose (Zykwinska et al ) or by the entrapment of pectins in or between cellulose microfibrils during wall biosynthesis (Phyo et al ). As a result, pectin–cellulose interactions may play an important role in wall biomechanical properties (Wang et al , Phyo et al ).…”

“…However, pectins also interact with cellulose microfibrils, either through binding of pectin side chains to cellulose (Zykwinska et al ) or by the entrapment of pectins in or between cellulose microfibrils during wall biosynthesis (Phyo et al ). As a result, pectin–cellulose interactions may play an important role in wall biomechanical properties (Wang et al , Phyo et al ). In growing inflorescence stems, a gradient of changes in pectin structures was correlated with reductions in wall compliances along the apical to basal gradient and a concomitant reduction in the ability of cells to undergo irreversible expansion (Phyo et al ).…”