Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR

Kang, Xue; Kirui, Alex; Dickwella Widanage, Malitha C.; Mentink-Vigier, Frederic; Cosgrove, Daniel J.; Wang, Tuo

doi:10.1038/s41467-018-08252-0

Title: Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR

Journal Article · 21 January 2019 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-08252-0 · OSTI ID:1566610

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^[2]; Cosgrove, Daniel J. ^[3];

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Louisiana State Univ., Baton Rouge, LA (United States)
Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
Pennsylvania State Univ., University Park, PA (United States)

Lignin is a complex aromatic biopolymer that strengthens and waterproofs plant secondary cell walls, enabling mechanical stability in trees and long-distance water transport in xylem. Lignin removal is a key step in paper production and biomass conversion to biofuels, motivating efforts to re-engineer lignin biosynthesis. However, the physical nature of lignin’s interactions with wall polysaccharides is not well understood. Here we show that lignin self-aggregates to form highly hydrophobic and dynamically unique nanodomains, with extensive surface contacts to xylan. Solid-state NMR spectroscopy of intact maize stems, supported by dynamic nuclear polarization, reveals that lignin has abundant electrostatic interactions with the polar motifs of xylan. Lignin preferentially binds xylans with 3-fold or distorted 2-fold helical screw conformations, indicative of xylans not closely associated with cellulose. These findings advance our knowledge of the molecular-level organization of lignocellulosic biomass, providing the structural foundation for optimization of post-harvest processing for biofuels and biomaterials.

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Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001090

OSTI ID:: 1566610

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Molecular architecture of softwood revealed by solid-state NMR Terrett, Oliver M.; Lyczakowski, Jan J.; Yu, Li Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12979-9	journal	October 2019
Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice Martin, Andri Fadillah; Tobimatsu, Yuki; Kusumi, Ryosuke Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53156-8	journal	November 2019
Designing xylan for improved sustainable biofuel production Oliveira, Dyoni M.; Mota, Thatiane R.; Salatta, Fábio V. Plant Biotechnology Journal, Vol. 17, Issue 12 https://doi.org/10.1111/pbi.13150	journal	July 2019
Structural Imaging of Native Cryo-Preserved Secondary Cell Walls Reveals the Presence of Macrofibrils and Their Formation Requires Normal Cellulose, Lignin and Xylan Biosynthesis. Lyczakowski, Jan J.; Bourdon, Matthieu; Terrett, Oliver M. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.46926	text	January 2019
Exploring the Treasure of Plant Molecules With Integrated Biorefineries Torres, Andres F.; Xu, Xuan; Nikiforidis, Constantinos V. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00478	journal	April 2019
Metabolomics: A Way Forward for Crop Improvement Razzaq, Ali; Sadia, Bushra; Raza, Ali Metabolites, Vol. 9, Issue 12 https://doi.org/10.3390/metabo9120303	journal	December 2019
A revised solid-state NMR method to assess the crystallinity of cellulose Sparrman, Tobias; Svenningsson, Leo; Sahlin-Sjövold, Karin Cellulose, Vol. 26, Issue 17 https://doi.org/10.1007/s10570-019-02718-0	journal	September 2019
Moisture-related changes in the nanostructure of woods studied with X-ray and neutron scattering Penttilä, Paavo A.; Altgen, Michael; Carl, Nico Cellulose, Vol. 27, Issue 1 https://doi.org/10.1007/s10570-019-02781-7	journal	October 2019
Structure, chemistry and physicochemistry of lignin for material functionalization Erfani Jazi, Mehdi; Narayanan, Ganesh; Aghabozorgi, Fatemeh SN Applied Sciences, Vol. 1, Issue 9 https://doi.org/10.1007/s42452-019-1126-8	journal	August 2019
Molecular architecture of softwood revealed by solid-state NMR Terrett, Oliver M.; Lyczakowski, Jan J.; Yu, Li Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12979-9	journal	October 2019
Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice Martin, Andri Fadillah; Tobimatsu, Yuki; Kusumi, Ryosuke Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-53156-8	journal	November 2019
A critical review on the analysis of lignin carbohydrate bonds Giummarella, Nicola; Pu, Yunqiao; Ragauskas, Arthur J. Green Chemistry, Vol. 21, Issue 7 https://doi.org/10.1039/c8gc03606c	journal	January 2019
Significant influence of lignin on axial elastic modulus of poplar wood at low microfibril angles under wet conditions Özparpucu, Merve; Gierlinger, Notburga; Cesarino, Igor Journal of Experimental Botany, Vol. 70, Issue 15 https://doi.org/10.1093/jxb/erz180	journal	April 2019
Designing xylan for improved sustainable biofuel production Oliveira, Dyoni M.; Mota, Thatiane R.; Salatta, Fábio V. Plant Biotechnology Journal, Vol. 17, Issue 12 https://doi.org/10.1111/pbi.13150	journal	July 2019
Molecular architecture of softwood revealed by solid-state NMR. Terrett, Oliver; Lyczakowski, Jan; Yu, Li Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.44837	text	January 2019
Molecular architecture of softwood revealed by solid-state NMR Terrett, Oliver M.; Lyczakowski, Jan J.; Yu, Li Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.59388	text	January 2019
Effects of Moisture on Diffusion in Unmodified Wood Cell Walls: A Phenomenological Polymer Science Approach Jakes, Joseph E.; Hunt, Christopher G.; Zelinka, Samuel L. Forests, Vol. 10, Issue 12 https://doi.org/10.3390/f10121084	journal	November 2019
Metabolomics: A Way Forward for Crop Improvement Razzaq, Ali; Sadia, Bushra; Raza, Ali Metabolites, Vol. 9, Issue 12 https://doi.org/10.3390/metabo9120303	journal	December 2019
Significant influence of lignin on axial elastic modulus of poplar wood at low microfibril angles under wet conditions Özparpucu, Merve; Gierlinger, Notburga; Cesarino, Igor ETH Zurich https://doi.org/10.3929/ethz-b-000361967	text	January 2019

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