Emergence of lignin-carbohydrate interactions during plant stem maturation visualized by solid-state NMR
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 carbohydr...
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Published in | Nature communications Vol. 16; no. 1; pp. 8010 - 15 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
27.08.2025
Nature Publishing Group Nature Portfolio |
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Online Access | Get full text |
ISSN | 2041-1723 2041-1723 |
DOI | 10.1038/s41467-025-63512-0 |
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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
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. |
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AbstractList | 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.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. 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. 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 C-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. 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.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. Lignification waterproofs and strengthens the secondary plant cell wall, while increasing the energy cost associated with releasing sugars for biofuel production. The physical association between lignin and the carbohydrate scaffold that accommodates lignin polymerization, as well as the temporally distinct roles of different lignin units and carbohydrate partners during lignification, remain largely unclear. Here we map the lignin-carbohydrate interactions by solid-state NMR in 13C-labeled Arabidopsis inflorescence stems as secondary cell walls are formed. Analysis includes wild-type and two mutants that either selectively or globally disrupt lignin biosynthesis. Mature cell walls in the basal regions of older stems are enriched in S-lignin and carbohydrate-lignin interactions. Acetylated xylan is the dominant mediator of interactions with S-lignin, while methylated pectin unexpectedly interacts with G-lignin during early-stage lignification. The critical role of S-lignin in stabilizing carbohydrate-lignin interface is emphasized by the weak lignin-carbohydrate interactions and compromised mechanical properties of a low-S fah1 mutant, whereas the ref3 mutant, with low overall lignin content but a higher S/G ratio, remained unaffected. These findings demonstrate that the molecular mixing pattern, rather than lignin content, is a key determinant of the structure and properties of lignocellulosic materials. 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. |
ArticleNumber | 8010 |
Author | Zhao, Wancheng Debnath, Debkumar Xiao, Peng Pfaff, Sarah A. Liu, Chang-Jun Wang, Tuo Vojvodin, Cameron S. Cosgrove, Daniel J. |
Author_xml | – sequence: 1 givenname: Peng orcidid: 0000-0002-6430-0278 surname: Xiao fullname: Xiao, Peng organization: Department of Chemistry, Michigan State University – sequence: 2 givenname: Sarah A. surname: Pfaff fullname: Pfaff, Sarah A. organization: Department of Biology, Pennsylvania State University – sequence: 3 givenname: Wancheng surname: Zhao fullname: Zhao, Wancheng organization: Department of Chemistry, Michigan State University, Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health – sequence: 4 givenname: Debkumar surname: Debnath fullname: Debnath, Debkumar organization: Department of Chemistry, Michigan State University – sequence: 5 givenname: Cameron S. surname: Vojvodin fullname: Vojvodin, Cameron S. organization: Department of Chemistry, Michigan State University – sequence: 6 givenname: Chang-Jun orcidid: 0000-0001-6189-8756 surname: Liu fullname: Liu, Chang-Jun organization: Biology Department, Brookhaven National Laboratory – sequence: 7 givenname: Daniel J. surname: Cosgrove fullname: Cosgrove, Daniel J. email: dcosgrove@psu.edu organization: Department of Biology, Pennsylvania State University – sequence: 8 givenname: Tuo orcidid: 0000-0002-1801-924X surname: Wang fullname: Wang, Tuo email: wangtuo1@msu.edu organization: Department of Chemistry, Michigan State University |
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Snippet | Lignification waterproofs and strengthens secondary plant cell walls but increases the energy cost of sugar release for biofuels. The physical association... Lignification waterproofs and strengthens the secondary plant cell wall, while increasing the energy cost associated with releasing sugars for biofuel... Abstract Lignification waterproofs and strengthens secondary plant cell walls but increases the energy cost of sugar release for biofuels. The physical... |
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SubjectTerms | 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 |
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Title | Emergence of lignin-carbohydrate interactions during plant stem maturation visualized by solid-state NMR |
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