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

Busse‐Wicher, Marta; Liu, An; Silveira, Rodrigo L.; Pereira, Caroline S.; Tryfona, Theodora; Gomes, Thiago C. F.; Skaf, Munir S.; Dupree, Paul

doi:10.1104/pp.16.00539

Cited by 149 publications

(175 citation statements)

References 63 publications

(84 reference statements)

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“…The presence of major domains with even distribution of the mGlcA units along the backbone and minor domains with uneven glucuronation was already reported in glucuronoxylan from Arabidopsis (Arabidopsis thaliana), which was ascribed to the action of two distinct glucuronyltransferases (Bromley et al, 2013). This structural information reveals that the intramolecular glycosylation pattern in AGX is more complex than reported previously (Busse-Wicher et al, 2016b). We here confirm (1) the relative abundance of regular motifs with even placement of Ara and mGlcA Domon and Costello, 1988).…”

Section: Differences In Substitution Pattern Between Xylan Populationsupporting

confidence: 75%

“…We have identified a major motif with a regular substitution pattern consisting of XXXXU m X and XXA 3 XU m X, with one mGlcA unit regularly placed every six Xyl units and an Ara moiety locked 22 units from the mGlcA, respectively. These oligosaccharide motifs also have been found in xylan extracted from the stem of other coniferous species (Busse-Wicher et al, 2016b), and their occurrence here is independently verified in softwoods from the genus Picea. This prevalent even spacing of substitutions in xylan had been proposed as well for acetylation in Arabidopsis glucuronoxylan (Busse-Wicher et al, 2014;Chong et al, 2014).…”

Section: Discussionmentioning

confidence: 68%

“…In particular, conifer xylans are of the arabinoglucuronoxylan (AGX) type, with a-(1→2) D-GlcA in its 4-O-methylated form (mGlcA) and a-(1→3) L-arabinofuranose (Ara) as the backbone main decorations and with no reported acetylations ( Fig. 1; Escalante et al, 2012;Busse-Wicher et al, 2016b;McKee et al, 2016). 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).…”

mentioning

confidence: 97%

“…Based on in silico predictions of NMR chemical shifts by density functional theory and MD simulations, this change has been identified as the transition from a 3 1 -fold helical structure to a flat 2 1 -fold screw (Busse-Wicher et al, 2016b;Simmons et al, 2016), which intuitively would facilitate close interaction between the xylan polymer and the flat cellulose surface, and even cocrystallization. Therefore, we initially placed the XOs in conformations that corresponded to the cellulose Ib structure (which constitute a 2 1 -fold screw) in an extra, hypothetical surface layer.…”

Section: Xylan Binding Onto Cellulose Hydrophilic and Hydrophobic Surmentioning

confidence: 99%

“…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).…”

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confidence: 99%

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

et al. 2017

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ORCID IDs: 0000-0003-0277-2269 (J.B.); 0000-0001-6732-2571 (J.W.); 0000-0003-3572-7798 (F.V.).Xylan is tightly associated with cellulose and lignin in secondary plant cell walls, contributing to its rigidity and structural integrity in vascular plants. However, the molecular features and the nanoscale forces that control the interactions among cellulose microfibrils, hemicelluloses, and lignin are still not well understood. Here, we combine comprehensive mass spectrometric glycan sequencing and molecular dynamics simulations to elucidate the substitution pattern in softwood xylans and to investigate the effect of distinct intramolecular motifs on xylan conformation and on the interaction with cellulose surfaces in Norway spruce (Picea abies). We confirm the presence of motifs with evenly spaced glycosyl decorations on the xylan backbone, together with minor motifs with consecutive glucuronation. These domains are differently enriched in xylan fractions extracted by alkali and subcritical water, which indicates their preferential positioning in the secondary plant cell wall ultrastructure. The flexibility of the 3-fold screw conformation of xylan in solution is enhanced by the presence of arabinofuranosyl decorations. Additionally, molecular dynamic simulations suggest that the glycosyl substitutions in xylan are not only sterically tolerated by the cellulose surfaces but that they increase the affinity for cellulose and favor the stabilization of the 2-fold screw conformation. This effect is more significant for the hydrophobic surface compared with the hydrophilic ones, which demonstrates the importance of nonpolar driving forces on the structural integrity of secondary plant cell walls. These novel molecular insights contribute to an improved understanding of the supramolecular architecture of plant secondary cell walls and have fundamental implications for overcoming lignocellulose recalcitrance and for the design of advanced wood-based materials.

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Section: Differences In Substitution Pattern Between Xylan Populationsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 68%

mentioning

confidence: 97%

Section: Xylan Binding Onto Cellulose Hydrophilic and Hydrophobic Surmentioning

confidence: 99%

mentioning

confidence: 99%

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

et al. 2017

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Revisiting the AA14 family of lytic polysaccharide monooxygenases and their catalytic activity

et al. 2023

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Lytic polysaccharide monooxygenases (LPMOs) belonging to the AA14 family are believed to contribute to the enzymatic degradation of lignocellulosic biomass by specifically acting on xylan in recalcitrant cellulose‐xylan complexes. Functional characterization of an AA14 LPMO from Trichoderma reesei, TrAA14A, and a re‐evaluation of the properties of the previously described AA14 from Pycnoporus coccineus, PcoAA14A, showed that these proteins have oxidase and peroxidase activities that are common for LPMOs. However, we were not able to detect activity on cellulose‐associated xylan or any other tested polysaccharide substrate, meaning that the substrate of these enzymes remains unknown. Next to raising questions regarding the true nature of AA14 LPMOs, the present data illustrate possible pitfalls in the functional characterization of these intriguing enzymes.

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Lignins and Lignification

Ralph¹,

Kim²,

Lu³

et al. 2023

Recent Advances in Polyphenol Research

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

Cited by 149 publications

References 63 publications

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

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

Revisiting the AA14 family of lytic polysaccharide monooxygenases and their catalytic activity

Lignins and Lignification

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