Xylan decoration patterns and the plant secondary cell wall molecular architecture

Abstract

The molecular architecture of plant secondary cell walls is still not resolved. There are several proposed structures for cellulose fibrils, the main component of plant cell walls and the conformation of other molecules is even less well known. Glucuronic acid (GlcA) substitution of xylan (GUX) enzymes, in CAZy family glycosyl transferase (GT)8, decorate the xylan backbone with various specific patterns of GlcA. It was recently discovered that dicot xylan has a domain with the side chain decorations distributed on every second unit of the backbone (xylose). If the xylan backbone folds in a similar way to glucan chains in cellulose (2-fold helix), this kind of arrangement may allow the undecorated side of the xylan chain to hydrogen bond with the hydrophilic surface of cellulose microfibrils. MD simulations suggest that such interactions are energetically stable. We discuss the possible role of this xylan decoration pattern in building of the plant cell wall.

Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR

“…Xn5 shifts are very similar to the solution state xylan Xn4 shift (Table 1), suggesting that they arise from threefold screw xylan in the cell wall, so we named them Xn4 3f and Xn5 3f , respectively. It has been proposed that some xylan may fold as twofold screw in the cell wall19202122. A change in torsion angle around the glycosidic bond (which yields different helical conformations) can alter the chemical shifts of polysaccharides, and in (1→4)-linked glycans changes in torsion angle has been shown to affect carbon 1 and carbon 4 resonances particularly27.…”

“…On the basis of a conserved pattern of xylan substitution strictly on alternate xylosyl residues, it has recently been proposed that xylan might be able to hydrogen bond to the hydrophilic surfaces of cellulose through folding as a twofold helical screw (Supplementary Fig. 2)19202122. This model is controversial because xylan in solution forms a threefold helical screw1923 (one 360° twist per three glycosidic bonds).…”

Evolution of Xylan Substitution Patterns in Gymnosperms and Angiosperms: Implications for Xylan Interaction with Cellulose

“…This xylan patterning is not restricted to acetylation and MeGlcA substitutions, but extends to arabinosyl residues too. We propose that the patterning of xylan substitutions allows a compatible interaction between xylan and the cellulose microfibril hydrophilic surfaces in vascular plants ( Busse-Wicher et al, 2014;Busse-Wicher et al, 2016).…”

Regular Motifs in Xylan Modulate Molecular Flexibility and Interactions with Cellulose Surfaces

“…Spatial and temporal heterogeneity in the composition and molecular structure of plant cell wall polysaccharides may be directed by biosynthetic processes in order to modulate their molecular diversity, adaptability, and biological function (Burton et al, 2010); however, the biological causes and effects of these fine structural variations are unknown. We are starting to understand how the molecular structure of hemicelluloses regulates the association with cellulose microfibrils (Bromley et al, 2013;Busse-Wicher et al, 2014, 2016a, 2016b and the occurrence of covalent linkages with lignins in lignin-carbohydrate complexes (Lawoko et al, 2005). The presence of intermolecular forces and the interconnected supramolecular architecture in lignocellulosic biomass are responsible for its recalcitrance against conversion into valuable biofuels and platform chemicals (Mortimer et al, 2010;Ding et al, 2012;Silveira et al, 2013).…”