The Patterned Structure of Galactoglucomannan Suggests It May Bind to Cellulose in Seed Mucilage

Abstract

The interaction between mannan polysaccharides and cellulose microfibrils contributes to cell wall properties in some vascular plants, but the molecular arrangement of mannan in the cell wall and the nature of the molecular bonding between mannan and cellulose remain unknown. Previous studies have shown that mannan is important in maintaining Arabidopsis () seed mucilage architecture, and that Cellulose Synthase-Like A2 (CSLA2) synthesizes a glucomannan backbone, which Mannan α-Galactosyl Transferase1 (MAGT1/GlycosylTransferase-Like6/Mucilage Related10) might decorate with single α-Gal branches. Here, we investigated the ratio and sequence of Man and Glc and the arrangement of Gal residues in Arabidopsis mucilage mannan using enzyme sequential digestion, carbohydrate gel electrophoresis, and mass spectrometry. We found that seed mucilage galactoglucomannan has a backbone consisting of the repeating disaccharide [4)-β-Glc-(1,4)-β-Man-(1,], and most of the Man residues in the backbone are substituted by single α-1,6-Gal. CSLA2 is responsible for the synthesis of this patterned glucomannan backbone and MAGT1 catalyses the addition of α-Gal. In vitro activity assays revealed that MAGT1 transferred α-Gal from UDP-Gal only to Man residues within the CSLA2 patterned glucomannan backbone acceptor. These results indicate that CSLAs and galactosyltransferases are able to make precisely defined galactoglucomannan structures. Molecular dynamics simulations suggested this patterned galactoglucomannan is able to bind stably to some hydrophilic faces and to hydrophobic faces of cellulose microfibrils. A specialization of the biosynthetic machinery to make galactoglucomannan with a patterned structure may therefore regulate the mode of binding of this hemicellulose to cellulose fibrils.

Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks

“…The presence of regular substitution patterns in wood mannans remains elusive 36 , although a recent study evidences that both xylans and mannans are intimately bound to cellulose surfaces in a semi-crystalline fashion in spruce wood 57 . It seems that an even placement of glucose and mannose units in the backbone of glucomannans benefits the interaction with cellulose surfaces 37,58 , and preliminary evidence of the occurrence of such motifs in spruce glucomannan has been recently reported 37 .…”

Enzymatic processing of lignocellulosic biomass: principles, recent advances and perspectives

“…Depending on the type of biomass and pretreatment technology, pretreated biomass contains, in addition to cellulose, varying amounts of linear and branched polysaccharides, including the hemicelluloses xylan, glucomannan and xyloglucan, as well as pectin, all of which adhere to cellulose fibers, forming a complex three-dimensional matrix [323]. These polysaccharides can form multiple substructures, and while many hemicelluloses are relatively easy to degrade, a fraction of these polysaccharides will form recalcitrant co-polymeric substructures that may hamper cellulose degradation [47,261,392]. Due to the high complexity of these plant polysaccharides, a variety of enzyme activities are needed for their complete breakdown ( Table 1).…”

Evolutionary origin of O‐acetyltransferases responsible for glucomannan acetylation in land plants

“…It has been shown that galactoglucomannan from the primary cell walls of ripe kiwifruit contains mannose, glucose and galactose in the molar ratio 2 : 2 : 1 (Schr€ oder et al, 2001). Galactoglucomannan with a similar molar ratio of mannose, glucose and galactose was also found in Arabidopsis seed mucilage (Voiniciuc et al, 2015;Yu et al, 2018).…”