The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana

Abstract

The interaction between xylan and cellulose microfibrils is important for secondary cell wall properties in vascular plants; however, the molecular arrangement of xylan in the cell wall and the nature of the molecular bonding between the polysaccharides are unknown. In dicots, the xylan backbone of β-(1,4)-linked xylosyl residues is decorated by occasional glucuronic acid, and approximately one-half of the xylosyl residues are O-acetylated at C-2 or C-3. We recently proposed that the even, periodic spacing of GlcA residues in the major domain of dicot xylan might allow the xylan backbone to fold as a twofold helical screw to facilitate alignment along, and stable interaction with, cellulose fibrils; however, such an interaction might be adversely impacted by random acetylation of the xylan backbone. Here, we investigated the arrangement of acetyl residues in Arabidopsis xylan using mass spectrometry and NMR. Alternate xylosyl residues along the backbone are acetylated. Using molecular dynamics simulation, we found that a twofold helical screw conformation of xylan is stable in interactions with both hydrophilic and hydrophobic cellulose faces. Tight docking of xylan on the hydrophilic faces is feasible only for xylan decorated on alternate residues and folded as a twofold helical screw. The findings suggest an explanation for the importance of acetylation for xylan–cellulose interactions, and also have implications for our understanding of cell wall molecular architecture and properties, and biological degradation by pathogens and fungi. They will also impact strategies to improve lignocellulose processing for biorefining and bioenergy.

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

“…3). Previous modeling studies show that the preferred conformation for xylan in solution is a twisted 3 1 -fold helical screw conformation (Mazeau et al, 2005;Busse-Wicher et al, 2014), the same as was reported previously for the experimentally determined crystal structure of xylan hydrate (Nieduszynski and Marchessault, 1971). Free energy surfaces for the backbone glycosidic linkage conformations are presented in Figure 4 (for X 6 and XXA 3 XU m X) and Supplemental Figure S9 (for all other glycosidic linkages).…”

“…A regular distribution of glucuronic acids was reported previously in the xylans extracted from softwoods, whereas the pattern in hardwoods seemed to be irregular (Jacobs et al, 2001). Recent studies, however, have shown that glycosidic and acetyl decorations are preferably evenly spaced in specific domains of the xylan backbone (Bromley et al, 2013;Busse-Wicher et al, 2014;Chong et al, 2014), which could sterically allow favorable interactions with the hydrophilic surfaces of cellulose microfibrils (BusseWicher et al, 2016a(BusseWicher et al, , 2016b. Moreover, backbone substitution influences the solubility of hemicelluloses and their macroscopic properties Sternemalm et al, 2008;Pitkänen et al, 2009;Escalante et al, 2012;Bosmans et al, 2014;Littunen et al, 2015).…”

“…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).…”

Two Trichome Birefringence-Like Proteins Mediate Xylan Acetylation, Which Is Essential for Leaf Blight Resistance in Rice

“…8A), which has not been reported in Arabidopsis. There, xylosyl residues were found to be alternatively substituted with acetates (Busse-Wicher et al, 2014). OsTBL2 shares 97% sequence identity with OsTBL1 (Supplemental Fig.…”

Cultura de células em suspensão como ferramenta para estudos em parede celular secundária em gramí­neas C4

“…O domínio fibrilar composto pelas microfibrilas de celulose encontra-se imerso no segundo domínio, formado por uma matriz de polissacarídeos não-celulósicos, as hemiceluloses e as pectinas, que conferem rigidez e resistência à parede (Buckeridge et al, 2000;Cosgrove, 2005). As hemiceluloses são formadas geralmente por um esqueleto de ligações β(1-4) com presença de cadeias laterais, que impedem a formação de estruturas cristalinas (Marriott et al, 2016), formando cadeias longas associadas à celulose através de pontes de hidrogênio (Busse-Wicher et al, 2014). Dependendo da espécie vegetal, as hemiceluloses representam de 20-40% dos polissacarídeos de parede celular (Marriott et al, 2016), podendo apresentar ainda composição variada.…”