A grass-specific cellulose–xylan interaction dominates in sorghum secondary cell walls
Abstract
Sorghum (Sorghum bicolor L. Moench) is a promising source of lignocellulosic biomass for the production of renewable fuels and chemicals, as well as for forage. Understanding secondary cell wall architecture is key to understanding recalcitrance i.e. identifying features which prevent the efficient conversion of complex biomass to simple carbon units. Here, we use multi-dimensional magic angle spinning solid-state NMR to characterize the sorghum secondary cell wall. We show that xylan is mainly in a three-fold screw conformation due to dense arabinosyl substitutions, with close proximity to cellulose. We also show that sorghum secondary cell walls present a high ratio of amorphous to crystalline cellulose as compared to dicots. We propose a model of sorghum cell wall architecture which is dominated by interactions between three-fold screw xylan and amorphous cellulose. This work will aid the design of low-recalcitrance biomass crops, a requirement for a sustainable bioeconomy.
- Publication Date:
- Research Org.:
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1724443
- Alternate Identifier(s):
- OSTI ID: 1728576; OSTI ID: 1765582
- Report Number(s):
- PNNL-SA-154449
Journal ID: ISSN 2041-1723; 6081; PII: 19837
- Grant/Contract Number:
- AC05-76RL01830; AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Name: Nature Communications Journal Volume: 11 Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; sorghum; secondary cell wall; xylan; arabinose; solid-state NMR; biofuels; plant physiology
Citation Formats
Gao, Yu, Lipton, Andrew S., Wittmer, Yuuki, Murray, Dylan T., and Mortimer, Jenny C.. A grass-specific cellulose–xylan interaction dominates in sorghum secondary cell walls. United Kingdom: N. p., 2020.
Web. doi:10.1038/s41467-020-19837-z.
Gao, Yu, Lipton, Andrew S., Wittmer, Yuuki, Murray, Dylan T., & Mortimer, Jenny C.. A grass-specific cellulose–xylan interaction dominates in sorghum secondary cell walls. United Kingdom. https://doi.org/10.1038/s41467-020-19837-z
Gao, Yu, Lipton, Andrew S., Wittmer, Yuuki, Murray, Dylan T., and Mortimer, Jenny C.. Fri .
"A grass-specific cellulose–xylan interaction dominates in sorghum secondary cell walls". United Kingdom. https://doi.org/10.1038/s41467-020-19837-z.
@article{osti_1724443,
title = {A grass-specific cellulose–xylan interaction dominates in sorghum secondary cell walls},
author = {Gao, Yu and Lipton, Andrew S. and Wittmer, Yuuki and Murray, Dylan T. and Mortimer, Jenny C.},
abstractNote = {Sorghum (Sorghum bicolor L. Moench) is a promising source of lignocellulosic biomass for the production of renewable fuels and chemicals, as well as for forage. Understanding secondary cell wall architecture is key to understanding recalcitrance i.e. identifying features which prevent the efficient conversion of complex biomass to simple carbon units. Here, we use multi-dimensional magic angle spinning solid-state NMR to characterize the sorghum secondary cell wall. We show that xylan is mainly in a three-fold screw conformation due to dense arabinosyl substitutions, with close proximity to cellulose. We also show that sorghum secondary cell walls present a high ratio of amorphous to crystalline cellulose as compared to dicots. We propose a model of sorghum cell wall architecture which is dominated by interactions between three-fold screw xylan and amorphous cellulose. This work will aid the design of low-recalcitrance biomass crops, a requirement for a sustainable bioeconomy.},
doi = {10.1038/s41467-020-19837-z},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United Kingdom},
year = {2020},
month = {11}
}
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Works referenced in this record:
High-level hemicellulosic arabinose predominately affects lignocellulose crystallinity for genetically enhancing both plant lodging resistance and biomass enzymatic digestibility in rice mutants
journal, November 2014
- Li, Fengcheng; Zhang, Mingliang; Guo, Kai
- Plant Biotechnology Journal, Vol. 13, Issue 4
Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants
journal, January 2013
- Wu, Zhiliang; Zhang, Mingliang; Wang, Lingqiang
- Biotechnology for Biofuels, Vol. 6, Issue 1
An Improved Broadband Decoupling Sequence for Liquid Crystals and Solids
journal, January 2000
- Fung, B. M.; Khitrin, A. K.; Ermolaev, Konstantin
- Journal of Magnetic Resonance, Vol. 142, Issue 1
Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls
journal, September 2015
- Wang, Tuo; Hong, Mei
- Journal of Experimental Botany, Vol. 67, Issue 2
A Brief and Informationally Rich Naming System for Oligosaccharide Motifs of Heteroxylans Found in Plant Cell Walls
journal, January 2009
- Fauré, Régis; Courtin, Christophe M.; Delcour, Jan A.
- Australian Journal of Chemistry, Vol. 62, Issue 6
Improvement of lignocellulosic biomass in planta: A review of feedstocks, biomass recalcitrance, and strategic manipulation of ideal plants designed for ethanol production and processability
journal, November 2013
- Phitsuwan, Paripok; Sakka, Kazuo; Ratanakhanokchai, Khanok
- Biomass and Bioenergy, Vol. 58
Current Understanding of the Correlation of Lignin Structure with Biomass Recalcitrance
journal, November 2016
- Li, Mi; Pu, Yunqiao; Ragauskas, Arthur J.
- Frontiers in Chemistry, Vol. 4
Hemicelluloses
journal, June 2010
- Scheller, Henrik Vibe; Ulvskov, Peter
- Annual Review of Plant Biology, Vol. 61, Issue 1
Xylan biosynthesis
journal, April 2014
- Rennie, Emilie A.; Scheller, Henrik Vibe
- Current Opinion in Biotechnology, Vol. 26
Structure and Dynamics of Brachypodium Primary Cell Wall Polysaccharides from Two-Dimensional 13 C Solid-State Nuclear Magnetic Resonance Spectroscopy
journal, April 2014
- Wang, Tuo; Salazar, Andre; Zabotina, Olga A.
- Biochemistry, Vol. 53, Issue 17
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
Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations
journal, May 2016
- Wang, Tuo; Yang, Hui; Kubicki, James D.
- Biomacromolecules, Vol. 17, Issue 6
The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana
journal, July 2014
- Busse-Wicher, Marta; Gomes, Thiago C. F.; Tryfona, Theodora
- The Plant Journal, Vol. 79, Issue 3
GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns
journal, March 2013
- Bromley, Jennifer R.; Busse-Wicher, Marta; Tryfona, Theodora
- The Plant Journal, Vol. 74, Issue 3
The Arabidopsis Golgi-localized GDP-L-fucose transporter is required for plant development
journal, July 2016
- Rautengarten, Carsten; Ebert, Berit; Liu, Lifeng
- Nature Communications, Vol. 7, Issue 1
Structure and Biogenesis of the cell Walls of Grasses
journal, June 1996
- Carpita, Nicholas C.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 47, Issue 1
Grass cell wall feruloylation: distribution of bound ferulate and candidate gene expression in Brachypodium distachyon
journal, January 2013
- Molinari, Hugo B. C.; Pellny, Till K.; Freeman, Jackie
- Frontiers in Plant Science, Vol. 4
13C–1H dipolar-assisted rotational resonance in magic-angle spinning NMR
journal, August 2001
- Takegoshi, K.; Nakamura, Shinji; Terao, Takehiko
- Chemical Physics Letters, Vol. 344, Issue 5-6
Xylan Biosynthesis: News from the Grass
journal, April 2010
- Faik, Ahmed
- Plant Physiology, Vol. 153, Issue 2
Covalent interactions between lignin and hemicelluloses in plant secondary cell walls
journal, April 2019
- Terrett, Oliver M.; Dupree, Paul
- Current Opinion in Biotechnology, Vol. 56
Maize Biomass Yield and Composition for Biofuels
journal, November 2007
- Dhugga, Kanwarpal S.
- Crop Science, Vol. 47, Issue 6
Tassel Removal Positively Affects Biomass Production Coupled with Significantly Increasing Stem Digestibility in Switchgrass
journal, April 2015
- Zhao, Chunqiao; Fan, Xifeng; Hou, Xincun
- PLOS ONE, Vol. 10, Issue 4
Cell wall cross-linking by ferulates and diferulates in grasses
journal, March 1999
- Hatfield, Ronald D.; Ralph, John; Grabber, John H.
- Journal of the Science of Food and Agriculture, Vol. 79, Issue 3
Lignin-polysaccharide interactions in plant secondary cell walls revealed by solid-state NMR
journal, January 2019
- Kang, Xue; Kirui, Alex; Dickwella Widanage, Malitha C.
- Nature Communications, Vol. 10, Issue 1
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose
journal, June 2016
- Busse-Wicher, Marta; Li, An; Silveira, Rodrigo L.
- Plant Physiology
Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls
journal, January 2004
- Ralph, John; Bunzel, Mirko; Marita, Jane M.
- Phytochemistry Reviews, Vol. 3, Issue 1-2, p. 79-96
A Fourier transform infra-red spectroscopic analysis of the character of hydrogen bonds in amorphous cellulose
journal, February 1996
- Kondo, Tetsuo; Sawatari, Chie
- Polymer, Vol. 37, Issue 3
Designer biomass for next-generation biorefineries: leveraging recent insights into xylan structure and biosynthesis
journal, November 2017
- Smith, Peter J.; Wang, Hsin-Tzu; York, William S.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Structure and Interactions of Plant Cell-Wall Polysaccharides by Two- and Three-Dimensional Magic-Angle-Spinning Solid-State NMR
journal, February 2011
- Dick-Pérez, Marilú; Zhang, Yuan; Hayes, Jennifer
- Biochemistry, Vol. 50, Issue 6
2016 Billion-Ton Report: Advancing Domestic Resources for a Thriving Bioeconomy
report, July 2016
- Langholtz, M. H.; Stokes, B. J.; Eaton, L. M.
- DOE/EE-1440
Toward a Systems Approach to Understanding Plant Cell Walls
journal, December 2004
- Somerville, C.
- Science, Vol. 306, Issue 5705
Probing the Molecular Architecture of Arabidopsis thaliana Secondary Cell Walls Using Two- and Three-Dimensional 13 C Solid State Nuclear Magnetic Resonance Spectroscopy
journal, March 2015
- Dupree, Ray; Simmons, Thomas J.; Mortimer, Jennifer C.
- Biochemistry, Vol. 54, Issue 14
Changes in Crystallinity of Cellulose During Dehydration
journal, May 1967
- Shimazu, F.; Sterling, C.
- Journal of Food Science, Vol. 32, Issue 3
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
Native Cellulose: A Composite of Two Distinct Crystalline Forms
journal, January 1984
- Atalla, R. H.; Vanderhart, D. L.
- Science, Vol. 223, Issue 4633
Genetic engineering of grass cell wall polysaccharides for biorefining
journal, June 2017
- Bhatia, Rakesh; Gallagher, Joe A.; Gomez, Leonardo D.
- Plant Biotechnology Journal, Vol. 15, Issue 9
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
The Shape of Native Plant Cellulose Microfibrils
journal, September 2018
- Kubicki, James D.; Yang, Hui; Sawada, Daisuke
- Scientific Reports, Vol. 8, Issue 1
Determination of Through-Bond Carbon−Carbon Connectivities in Solid-State NMR Using the INADEQUATE Experiment
journal, August 1997
- Lesage, Anne; Auger, Céline; Caldarelli, Stefano
- Journal of the American Chemical Society, Vol. 119, Issue 33
Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis
journal, November 2016
- Fang, Lin; Ishikawa, Toshiki; Rennie, Emilie A.
- The Plant Cell, Vol. 28, Issue 12
Redesigning plant cell walls for the biomass-based bioeconomy
journal, August 2020
- Carpita, Nicholas C.; McCann, Maureen C.
- Journal of Biological Chemistry, Vol. 295, Issue 44
Oligosaccharides as Signals and Substrates in the Plant Cell Wall
journal, September 1993
- Fry, S. C.; Aldington, S.; Hetherington, P. R.
- Plant Physiology, Vol. 103, Issue 1
Complete Resonance Assignment of a Natural Abundance Solid Peptide by Through-Bond Heteronuclear Correlation Solid-State NMR
journal, October 2000
- Lesage, Anne; Charmont, Patrick; Steuernagel, Stefan
- Journal of the American Chemical Society, Vol. 122, Issue 40
An assessment of the potential products and economic and environmental impacts resulting from a billion ton bioeconomy
journal, November 2016
- Rogers, Jonathan N.; Stokes, Bryce; Dunn, Jennifer
- Biofuels, Bioproducts and Biorefining, Vol. 11, Issue 1
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
Designing sorghum as a dedicated bioenergy feedstock
journal, October 2007
- Rooney, William L.; Blumenthal, Jürg; Bean, Brent
- Biofuels, Bioproducts and Biorefining, Vol. 1, Issue 2
Effects of Pectin Molecular Weight Changes on the Structure, Dynamics, and Polysaccharide Interactions of Primary Cell Walls of Arabidopsis thaliana : Insights from Solid-State NMR
journal, August 2017
- Phyo, Pyae; Wang, Tuo; Xiao, Chaowen
- Biomacromolecules, Vol. 18, Issue 9
Pectin–Cellulose Interactions in the Arabidopsis Primary Cell Wall from Two-Dimensional Magic-Angle-Spinning Solid-State Nuclear Magnetic Resonance
journal, November 2012
- Wang, Tuo; Zabotina, Olga; Hong, Mei
- Biochemistry, Vol. 51, Issue 49
Genetic modification of plant cell walls to enhance biomass yield and biofuel production in bioenergy crops
journal, September 2016
- Wang, Yanting; Fan, Chunfen; Hu, Huizhen
- Biotechnology Advances, Vol. 34, Issue 5
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
Molecular architecture of softwood revealed by solid-state NMR
journal, October 2019
- Terrett, Oliver M.; Lyczakowski, Jan J.; Yu, Li
- Nature Communications, Vol. 10, Issue 1
The role of solid state NMR spectroscopy in studies of the nature of native celluloses
journal, October 1999
- Atalla, R. H.; VanderHart, D. L.
- Solid State Nuclear Magnetic Resonance, Vol. 15, Issue 1
Ramped-Amplitude Cross Polarization in Magic-Angle-Spinning NMR
journal, October 1994
- Metz, G.; Wu, X. L.; Smith, S. O.
- Journal of Magnetic Resonance, Series A, Vol. 110, Issue 2
Sugar-rich sweet sorghum is distinctively affected by wall polymer features for biomass digestibility and ethanol fermentation in bagasse
journal, September 2014
- Li, Meng; Feng, Shengqiu; Wu, Leiming
- Bioresource Technology, Vol. 167
High biomass yield energy sorghum: developing a genetic model for C4 grass bioenergy crops: Modeling and Analysis: Developing a genetic model for C4 grass bioenergy crops
journal, September 2012
- Olson, Sara N.; Ritter, Kimberley; Rooney, William
- Biofuels, Bioproducts and Biorefining, Vol. 6, Issue 6
Through-Bond Carbon−Carbon Connectivities in Disordered Solids by NMR
journal, December 1999
- Lesage, Anne; Bardet, Michel; Emsley, Lyndon
- Journal of the American Chemical Society, Vol. 121, Issue 47
Arabinose substitution degree in xylan positively affects lignocellulose enzymatic digestibility after various NaOH/H2SO4 pretreatments in Miscanthus
journal, February 2013
- Li, Fengcheng; Ren, Shuangfeng; Zhang, Wei
- Bioresource Technology, Vol. 130
Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass
journal, September 2010
- Mortimer, J. C.; Miles, G. P.; Brown, D. M.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 40
Unique aspects of the grass cell wall
journal, June 2008
- Vogel, J.
- Current Opinion in Plant Biology, Vol. 11, Issue 3
Genetic and molecular basis of grass cell-wall degradability. I. Lignin–cell wall matrix interactions
journal, May 2004
- Grabber, John H.; Ralph, John; Lapierre, Catherine
- Comptes Rendus Biologies, Vol. 327, Issue 5