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

Abstract

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.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2];  [3]; ORCiD logo [1]
+ Show Author Affiliations
  1. Louisiana State Univ., Baton Rouge, LA (United States)
  2. Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)
  3. Pennsylvania State Univ., University Park, PA (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF); Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1566610
Grant/Contract Number:  
SC0001090
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biofuels (including algae and biomass); bio-inspired; membrane; carbon sequestration; materials and chemistry by design; synthesis (self-assembly)

Citation Formats

Kang, Xue, Kirui, Alex, Dickwella Widanage, Malitha C., Mentink-Vigier, Frederic, Cosgrove, Daniel J., and Wang, Tuo. Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR. United States: N. p., 2019. Web. doi:10.1038/s41467-018-08252-0.
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Kang, Xue, Kirui, Alex, Dickwella Widanage, Malitha C., Mentink-Vigier, Frederic, Cosgrove, Daniel J., & Wang, Tuo. Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR. United States. https://doi.org/10.1038/s41467-018-08252-0
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Kang, Xue, Kirui, Alex, Dickwella Widanage, Malitha C., Mentink-Vigier, Frederic, Cosgrove, Daniel J., and Wang, Tuo. Mon . "Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR". United States. https://doi.org/10.1038/s41467-018-08252-0. https://www.osti.gov/servlets/purl/1566610.
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@article{osti_1566610,
title = {Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR},
author = {Kang, Xue and Kirui, Alex and Dickwella Widanage, Malitha C. and Mentink-Vigier, Frederic and Cosgrove, Daniel J. and Wang, Tuo},
abstractNote = {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.},
doi = {10.1038/s41467-018-08252-0},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {Mon Jan 21 00:00:00 EST 2019},
month = {Mon Jan 21 00:00:00 EST 2019}
}
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https://doi.org/10.1038/s41467-018-08252-0
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Works referenced in this record:

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Feedstocks for Lignocellulosic Biofuels
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An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls
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Highly Efficient, Water-Soluble Polarizing Agents for Dynamic Nuclear Polarization at High Frequency
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Secondary Structure, Dynamics, and Topology of a Seven-Helix Receptor in Native Membranes, Studied by Solid-State NMR Spectroscopy
journal, January 2007

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Ultra-structural organisation of cell wall polymers in normal and tension wood of aspen revealed by polarisation FTIR microspectroscopy
journal, February 2011

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journal, October 2012

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Relaxation-compensated difference spin diffusion NMR for detecting 13C–13C long-range correlations in proteins and polysaccharides
journal, December 2014

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journal, September 2004

The refocused INADEQUATE MAS NMR experiment in multiple spin-systems: Interpreting observed correlation peaks and optimising lineshapes
journal, September 2007

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Mechanisms of dynamic nuclear polarization in insulating solids
journal, April 2015

Aromatic spectral editing techniques for magic-angle-spinning solid-state NMR spectroscopy of uniformly 13C-labeled proteins
journal, November 2015

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journal, March 2013

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journal, April 2013

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journal, December 2005

  • Elena, Bénédicte; Lesage, Anne; Steuernagel, Stefan
  • Journal of the American Chemical Society, Vol. 127, Issue 49
  • DOI: 10.1021/ja054411x

Water–Polysaccharide Interactions in the Primary Cell Wall of Arabidopsis thaliana from Polarization Transfer Solid-State NMR
journal, July 2014

  • White, Paul B.; Wang, Tuo; Park, Yong Bum
  • Journal of the American Chemical Society, Vol. 136, Issue 29
  • DOI: 10.1021/ja504108h

Cross-Linking of Maize Walls by Ferulate Dimerization and Incorporation into Lignin
journal, December 2000

  • Grabber, John H.; Ralph, John; Hatfield, Ronald D.
  • Journal of Agricultural and Food Chemistry, Vol. 48, Issue 12, p. 6106-6113
  • DOI: 10.1021/jf0006978

Molecular Modeling of the Structural and Dynamical Properties of Secondary Plant Cell Walls: Influence of Lignin Chemistry
journal, March 2012

  • Charlier, Landry; Mazeau, Karim
  • The Journal of Physical Chemistry B, Vol. 116, Issue 14
  • DOI: 10.1021/jp300395k

Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014

  • Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
  • Nature, Vol. 509, Issue 7500, p. 376-380
  • DOI: 10.1038/nature13084

Molecular architecture of fungal cell walls revealed by solid-state NMR
journal, July 2018

An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls
journal, October 2017

  • Grantham, Nicholas J.; Wurman-Rodrich, Joel; Terrett, Oliver M.
  • Nature Plants, Vol. 3, Issue 11
  • DOI: 10.1038/s41477-017-0030-8

Nanostructure of cellulose microfibrils in spruce wood
journal, November 2011

  • Fernandes, A. N.; Thomas, L. H.; Altaner, C. M.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 47
  • DOI: 10.1073/pnas.1108942108

Cellulose-Lignin Interactions (A Computational Study)
journal, March 1995

Cellulose-Pectin Spatial Contacts Are Inherent to Never-Dried Arabidopsis Primary Cell Walls: Evidence from Solid-State Nuclear Magnetic Resonance
journal, June 2015

  • Wang, Tuo; Park, Yong Bum; Cosgrove, Daniel J.
  • Plant Physiology, Vol. 168, Issue 3
  • DOI: 10.1104/pp.15.00665

Energy metabolism of Plantago lanceolata, as affected by change in root temperature
journal, September 1982

Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks
journal, July 2014

  • Poovaiah, Charleson R.; Nageswara-Rao, Madhugiri; Soneji, Jaya R.
  • Plant Biotechnology Journal, Vol. 12, Issue 9
  • DOI: 10.1111/pbi.12225

Feedstocks for Lignocellulosic Biofuels
journal, August 2010

  • Somerville, Cris; Youngs, Heather; Taylor, Caroline
  • Science, Vol. 329, Issue 5993, p. 790-792
  • DOI: 10.1126/science.1189268

CELLULOSIC ETHANOL: Biofuel Researchers Prepare to Reap a New Harvest
journal, March 2007

Proposed supramolecular structure of lignin in softwood tracheid compound middle lamella regions
journal, December 2012

  • Terashima, Noritsugu; Yoshida, Masato; Hafrén, Jonas
  • Holzforschung, Vol. 66, Issue 8
  • DOI: 10.1515/hf-2012-0021

A review of xylan and lignin biosynthesis: Foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes
journal, February 2014

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    Tailoring NMR experiments for structural characterization of amorphous biological solids: A practical guide
    journal, October 2020

    • Kelly, John E.; Chrissian, Christine; Stark, Ruth E.
    • Solid State Nuclear Magnetic Resonance, Vol. 109
    • DOI: 10.1016/j.ssnmr.2020.101686

    Molecular architecture of softwood revealed by solid-state NMR
    journal, October 2019

    Altered lignocellulose chemical structure and molecular assembly in CINNAMYL ALCOHOL DEHYDROGENASE-deficient rice
    journal, November 2019

    Designing xylan for improved sustainable biofuel production
    journal, July 2019

    • Oliveira, Dyoni M.; Mota, Thatiane R.; Salatta, Fábio V.
    • Plant Biotechnology Journal, Vol. 17, Issue 12
    • DOI: 10.1111/pbi.13150

    Exploring the Treasure of Plant Molecules With Integrated Biorefineries
    journal, April 2019

    • Torres, Andres F.; Xu, Xuan; Nikiforidis, Constantinos V.
    • Frontiers in Plant Science, Vol. 10
    • DOI: 10.3389/fpls.2019.00478

    Metabolomics: A Way Forward for Crop Improvement
    journal, December 2019

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