An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls

Abstract

Xylan and cellulose are abundant polysaccharides in vascular plants and essential for secondary cell wall strength. Acetate or glucuronic acid decorations are exclusively found on even-numbered residues in most of the glucuronoxylan polymer. It has been proposed that this even-specific positioning of the decorations might permit docking of xylan onto the hydrophilic face of a cellulose microfibril . Consequently, xylan adopts a flattened ribbon-like twofold screw conformation when bound to cellulose in the cell wall . Here we show that ESKIMO1/XOAT1/TBL29, a xylan-specific O-acetyltransferase, is necessary for generation of the even pattern of acetyl esters on xylan in Arabidopsis. The reduced acetylation in the esk1 mutant deregulates the position-specific activity of the xylan glucuronosyltransferase GUX1, and so the even pattern of glucuronic acid on the xylan is lost. Solid-state NMR of intact cell walls shows that, without the even-patterned xylan decorations, xylan does not interact normally with cellulose fibrils. We conclude that the even pattern of xylan substitutions seen across vascular plants enables the interaction of xylan with hydrophilic faces of cellulose fibrils, and is essential for development of normal plant secondary cell walls.

Monitoring Polysaccharide Dynamics in the Plant Cell Wall

“…Xylans were found to have a flattened conformation and were bound closely to cellulose microfibrils in wild-type Arabidopsis stems but not in a cellulose-deficient mutant (Simmons et al, 2016). Moreover, solid-state NMR revealed that an even pattern of substitution is essential for xylan to bind to cellulose in the 2-fold screw conformation (Grantham et al, 2017). The role of these regular motifs also is supported by mass spectrometric sequencing and molecular dynamics simulations of xylan oligomers (Martínez-Abad et al, 2017).…”

Exploiting CELLULOSE SYNTHASE (CESA) Class Specificity to Probe Cellulose Microfibril Biosynthesis

“…This is likely to mask more subtle changes in microfibril structure 427 that may exist within the various classes of mutants we have identified. In the future, it may be 428 necessary to use more sensitive techniques, such as two-dimensional ssNMR, to closely examine 429 both microfibril structure and also the interaction between the microfibrils and the xylan that is 430 bound to them (Dupree et al, 2015;Grantham et al, 2017 …”

Growth‐ and stress‐related defects associated with wall hypoacetylation are strigolactone‐dependent

“…The physiochemical properties of the secondary wall depend on the structure of the polymers (mainly cellulose, xylan and lignin) forming these walls. The degree of O‐acetylation of xylan, the major acetylated polymer in secondary walls, seems to have a strong impact on these properties affecting the xylan‐cellulose interaction (Ebringerová, Hromádková, & Heinze, ; Grantham et al., ). Although the biological significance of this modification is not clear, single and multiple mutants characterized in several plant species have shown a strong correlation between the level of reduction in xylan acetylation and a stunted plant growth and xylem collapse.…”