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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]
  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.
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. doi:10.1038/s41467-018-08252-0.
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. doi:10.1038/s41467-018-08252-0. https://www.osti.gov/servlets/purl/1566610.
@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 = {2019},
month = {1}
}

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Works referenced in this record:

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


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

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

Raman Microprobe Evidence for Lignin Orientation in the Cell Walls of Native Woody Tissue
journal, February 1985


Lignification and lignin topochemistry — an ultrastructural view
journal, July 2001


Modelling one- and two-dimensional solid-state NMR spectra: Modelling 1D and 2D solid-state NMR spectra
journal, December 2001

  • Massiot, Dominique; Fayon, Franck; Capron, Mickael
  • Magnetic Resonance in Chemistry, Vol. 40, Issue 1
  • DOI: 10.1002/mrc.984

Secondary Structure, Dynamics, and Topology of a Seven-Helix Receptor in Native Membranes, Studied by Solid-State NMR Spectroscopy
journal, January 2007

  • Etzkorn, Manuel; Martell, Swetlana; Andronesi, Ovidiu C.
  • Angewandte Chemie International Edition, Vol. 46, Issue 3
  • DOI: 10.1002/anie.200602139

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

Comparative structure and biomechanics of plant primary and secondary cell walls
journal, January 2012


Spectral editing of two-dimensional magic-angle-spinning solid-state NMR spectra for protein resonance assignment and structure determination
journal, October 2012

  • Schmidt-Rohr, K.; Fritzsching, K. J.; Liao, S. Y.
  • Journal of Biomolecular NMR, Vol. 54, Issue 4
  • DOI: 10.1007/s10858-012-9676-8

Is solid-state NMR enhanced by dynamic nuclear polarization?
journal, April 2015


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


Highly Efficient, Water-Soluble Polarizing Agents for Dynamic Nuclear Polarization at High Frequency
journal, August 2013

  • Sauvée, Claire; Rosay, Melanie; Casano, Gilles
  • Angewandte Chemie International Edition, Vol. 52, Issue 41
  • DOI: 10.1002/anie.201304657

High Frequency Dynamic Nuclear Polarization
journal, April 2013

  • Ni, Qing Zhe; Daviso, Eugenio; Can, Thach V.
  • Accounts of Chemical Research, Vol. 46, Issue 9
  • DOI: 10.1021/ar300348n

Engineering of plant cell walls for enhanced biofuel production
journal, June 2015

  • Loqué, Dominique; Scheller, Henrik V.; Pauly, Markus
  • Current Opinion in Plant Biology, Vol. 25
  • DOI: 10.1016/j.pbi.2015.05.018

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


The Path Forward for Biofuels and Biomaterials
journal, January 2006

  • Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H.
  • Science, Vol. 311, Issue 5760, p. 484-489
  • DOI: 10.1126/science.1114736

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

Model Studies of Ferulate−Coniferyl Alcohol Cross-Product Formation in Primary Maize Walls:  Implications for Lignification in Grasses
journal, October 2002

  • Grabber, John H.; Ralph, John; Hatfield, Ronald D.
  • Journal of Agricultural and Food Chemistry, Vol. 50, Issue 21, p. 6008-6016
  • DOI: 10.1021/jf0205312

Practical aspects of high-sensitivity multidimensional 13C MAS NMR spectroscopy of perdeuterated proteins
journal, April 2012

  • Akbey, Ümit; Rossum, Barth-Jan van; Oschkinat, Hartmut
  • Journal of Magnetic Resonance, Vol. 217
  • DOI: 10.1016/j.jmr.2012.02.015

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

Molecular Modeling and Imaging of Initial Stages of Cellulose Fibril Assembly: Evidence for a Disordered Intermediate Stage
journal, April 2014


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


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

  • Wang, Tuo; Williams, Jonathan K.; Schmidt-Rohr, Klaus
  • Journal of Biomolecular NMR, Vol. 61, Issue 2
  • DOI: 10.1007/s10858-014-9889-0

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

Common processes drive the thermochemical pretreatment of lignocellulosic biomass
journal, January 2014

  • Langan, Paul; Petridis, Loukas; O'Neill, Hugh M.
  • Green Chem., Vol. 16, Issue 1
  • DOI: 10.1039/C3GC41962B

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


Solution-State 2D NMR Spectroscopy of Plant Cell Walls Enabled by a Dimethylsulfoxide- d 6 /1-Ethyl-3-methylimidazolium Acetate Solvent
journal, March 2013

  • Cheng, Kun; Sorek, Hagit; Zimmermann, Herbert
  • Analytical Chemistry, Vol. 85, Issue 6
  • DOI: 10.1021/ac303529v

Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012


Dynamic Nuclear Polarization Surface Enhanced NMR Spectroscopy
journal, March 2013

  • Rossini, Aaron J.; Zagdoun, Alexandre; Lelli, Moreno
  • Accounts of Chemical Research, Vol. 46, Issue 9
  • DOI: 10.1021/ar300322x

Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR
journal, December 2016

  • Simmons, Thomas J.; Mortimer, Jenny C.; Bernardinelli, Oigres D.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13902

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

  • Cadars, Sylvian; Sein, Julien; Duma, Luminita
  • Journal of Magnetic Resonance, Vol. 188, Issue 1
  • DOI: 10.1016/j.jmr.2007.05.016

Micromechanical understanding of the cell-wall structure
journal, September 2004


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


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

Aggregation during Coniferyl Alcohol Polymerization in Pectin Solution:  A Biomimetic Approach of the First Steps of Lignification
journal, March 2005

  • Lairez, D.; Cathala, B.; Monties, B.
  • Biomacromolecules, Vol. 6, Issue 2
  • DOI: 10.1021/bm049390y

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

  • Williams, Jonathan K.; Schmidt-Rohr, Klaus; Hong, Mei
  • Solid State Nuclear Magnetic Resonance, Vol. 72
  • DOI: 10.1016/j.ssnmr.2015.09.006

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

Atomic-Level Structure Characterization of Biomass Pre- and Post-Lignin Treatment by Dynamic Nuclear Polarization-Enhanced Solid-State NMR
journal, January 2017

  • Perras, Frédéric A.; Luo, Hao; Zhang, Ximing
  • The Journal of Physical Chemistry A, Vol. 121, Issue 3
  • DOI: 10.1021/acs.jpca.6b11121

Fractionation and Characterization of Completely Dissolved Ball Milled Hardwood
journal, July 2011


Biodegradation of lignin-carbohydrate complexes
journal, January 1990


Atomic resolution of cotton cellulose structure enabled by dynamic nuclear polarization solid-state NMR
journal, November 2018


Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants
journal, September 2016

  • Li, Shundai; Bashline, Logan; Zheng, Yunzhen
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 40
  • DOI: 10.1073/pnas.1613273113

Broadband homonuclear correlation spectroscopy driven by combined <mml:math altimg="si1.gif" overflow="scroll" xmlns:xocs="http://www.elsevier.com/xml/xocs/dtd" xmlns:xs="http://www.w3.org/2001/XMLSchema" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xmlns="http://www.elsevier.com/xml/ja/dtd" xmlns:ja="http://www.elsevier.com/xml/ja/dtd" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:tb="http://www.elsevier.com/xml/common/table/dtd" xmlns:sb="http://www.elsevier.com/xml/common/struct-bib/dtd" xmlns:ce="http://www.elsevier.com/xml/common/dtd" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:cals="http://www.elsevier.com/xml/common/cals/dtd" xmlns:sa="http://www.elsevier.com/xml/common/struct-aff/dtd"><mml:mrow><mml:mtext>R</mml:mtext><mml:msubsup><mml:mrow><mml:mn>2</mml:mn></mml:mrow><mml:mrow><mml:mi>n</mml:mi></mml:mrow><mml:mrow><mml:mi>v</mml:mi></mml:mrow></mml:msubsup></mml:mrow></mml:math> sequences under fast magic angle spinning for NMR structural analysis of organic and biological solids
journal, July 2013


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

Proton to Carbon-13 INEPT in Solid-State NMR Spectroscopy
journal, December 2005

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

Lignin engineering
journal, June 2008

  • Vanholme, R.; Morreel, K.; Ralph, J.
  • Current Opinion in Plant Biology, Vol. 11, Issue 3, p. 278-285
  • DOI: 10.1016/j.pbi.2008.03.005

Protein dynamics by solid-state NMR: aromatic rings of the coat protein in fd bacteriophage.
journal, January 1982

  • Gall, C. M.; Cross, T. A.; DiVerdi, J. A.
  • Proceedings of the National Academy of Sciences, Vol. 79, Issue 1
  • DOI: 10.1073/pnas.79.1.101

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

    Works referencing / citing this record:

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


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


    A revised solid-state NMR method to assess the crystallinity of cellulose
    journal, September 2019


    Moisture-related changes in the nanostructure of woods studied with X-ray and neutron scattering
    journal, October 2019


    Structure, chemistry and physicochemistry of lignin for material functionalization
    journal, August 2019

    • Erfani Jazi, Mehdi; Narayanan, Ganesh; Aghabozorgi, Fatemeh
    • SN Applied Sciences, Vol. 1, Issue 9
    • DOI: 10.1007/s42452-019-1126-8

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


    A critical review on the analysis of lignin carbohydrate bonds
    journal, January 2019

    • Giummarella, Nicola; Pu, Yunqiao; Ragauskas, Arthur J.
    • Green Chemistry, Vol. 21, Issue 7
    • DOI: 10.1039/c8gc03606c

    Significant influence of lignin on axial elastic modulus of poplar wood at low microfibril angles under wet conditions
    journal, April 2019

    • Özparpucu, Merve; Gierlinger, Notburga; Cesarino, Igor
    • Journal of Experimental Botany, Vol. 70, Issue 15
    • DOI: 10.1093/jxb/erz180

    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

    Effects of Moisture on Diffusion in Unmodified Wood Cell Walls: A Phenomenological Polymer Science Approach
    journal, November 2019

    • Jakes, Joseph E.; Hunt, Christopher G.; Zelinka, Samuel L.
    • Forests, Vol. 10, Issue 12
    • DOI: 10.3390/f10121084

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