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

• Published in: Nature communications Vol. 16; no. 1; pp. 8010 - 15
• Main Authors: Xiao, Peng, Pfaff, Sarah A., Zhao, Wancheng, Debnath, Debkumar, Vojvodin, Cameron S., Liu, Chang-Jun, Cosgrove, Daniel J., Wang, Tuo
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 27.08.2025; Nature Publishing Group; Nature Portfolio
• Subjects: 101/6; 140/131; 631/449/448/1365; 631/535/878/1264; 639/638/45/72/1205; Alternative energy sources; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; BASIC BIOLOGICAL SCIENCES; Biofuels; Biosynthesis; Carbohydrate Metabolism; Carbohydrates; Carbohydrates - chemistry; Carbon; Cell Wall - metabolism; Cell walls; Cellulose; Energy costs; Enzymes; Humanities and Social Sciences; Lignin; Lignin - chemistry; Lignin - metabolism; Lignocellulose; Magnetic Resonance Spectroscopy - methods; Mechanical properties; multidisciplinary; Mutants; Mutation; NMR; Nuclear magnetic resonance; Pectin; Pectins - metabolism; Plant Stems - growth & development; Plant Stems - metabolism; Science; Science (multidisciplinary); Solid state; Spectrum analysis; Stems; Xylan; Xylans - metabolism
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-025-63512-0

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 13 C-labeled Arabidopsi s 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. Solid-state NMR reveals that lignin-carbohydrate contact patterns, rather than lignin amount, shape the structure and property of plant cell walls, highlighting distinct roles of lignin and carbohydrate units during wall formation.