Emergence of lignin-carbohydrate interactions during plant stem maturation visualized by solid-state NMR

Peng Xiao, Sarah A. Pfaff, Wancheng Zhao, Debkumar Debnath, Cameron S. Vojvodin, Chang-Jun Liu, Daniel J. Cosgrove () and Tuo Wang ()
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Peng Xiao: Michigan State University
Sarah A. Pfaff: Pennsylvania State University
Wancheng Zhao: Michigan State University
Debkumar Debnath: Michigan State University
Cameron S. Vojvodin: Michigan State University
Chang-Jun Liu: Brookhaven National Laboratory
Daniel J. Cosgrove: Pennsylvania State University
Tuo Wang: Michigan State University

Nature Communications, 2025, vol. 16, issue 1, 1-15

Abstract: Abstract Lignification waterproofs and strengthens secondary plant cell walls but increases the energy cost of sugar release for biofuels. The physical association between lignin and the carbohydrate scaffold that accommodates lignin polymerization, along with the distinct roles of lignin units and carbohydrate partners during lignification, remain unclear. Here, we map lignin-carbohydrate spatial proximity by solid-state NMR in 13C-labeled Arabidopsis inflorescence stems during secondary cell wall formation. Analyses include wild-type plants and mutants that selectively or globally disrupt lignin biosynthesis. Mature walls in basal regions show enrichment of S-lignin and dense carbohydrate-lignin packing. Acetylated xylan predominantly associates with S-lignin, while methylated pectin unexpectedly interacts with G-lignin during early-stage lignification. The importance of S-lignin in stabilizing the carbohydrate-lignin interface is highlighted by weak lignin-carbohydrate contacts and compromised mechanical properties in the low-S fah1 mutant, whereas the ref3 mutant, despite reduced lignin content, remains unaffected due to a high S/G ratio. Thus, molecular mixing patterns, rather than lignin content, critically determine the structure and properties of lignocellulosic materials.

Date: 2025
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DOI: 10.1038/s41467-025-63512-0

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