Multidimensional solid-state NMR spectroscopy of plant cell walls

doi:10.1016/j.ssnmr.2016.08.001

Title: Multidimensional solid-state NMR spectroscopy of plant cell walls

Full Record
Other Related Research

Abstract

Plant biomass has become an important source of bio-renewable energy in modern society. The molecular structure of plant cell walls is difficult to characterize by most atomic-resolution techniques due to the insoluble and disordered nature of the cell wall. Solid-state NMR (SSNMR) spectroscopy is uniquely suited for studying native hydrated plant cell walls at the molecular level with chemical resolution. Significant progress has been made in the last five years to elucidate the molecular structures and interactions of cellulose and matrix polysaccharides in plant cell walls. These studies have focused on primary cell walls of growing plants in both the dicotyledonous and grass families, as represented by the model plants Arabidopsis thaliana, Brachypodium distachyon, and Zea mays. To date, these SSNMR results have shown that 1) cellulose, hemicellulose, and pectins form a single network in the primary cell wall; 2) in dicot cell walls, the protein expansin targets the hemicellulose-enriched region of the cellulose microfibril for its wall-loosening function; and 3) primary wall cellulose has polymorphic structures that are distinct from the microbial cellulose structures. This article summarizes these key findings, and points out future directions of investigation to advance our fundamental understanding of plant cell wall structure and function.

Authors:

Wang, Tuo ^[1]; Phyo, Pyae ^[1]; Hong, Mei ^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Chemistry

Publication Date:: 2016-09-01

Research Org.:: Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)

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

OSTI Identifier:: 1388014

Alternate Identifier(s):: OSTI ID: 1397044

Grant/Contract Number:: SC0001090

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Solid State Nuclear Magnetic Resonance

Additional Journal Information:: Journal Volume: 78; Journal Issue: C; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; Journal ID: ISSN 0926-2040

Publisher:: Elsevier

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Wang, Tuo, Phyo, Pyae, and Hong, Mei. Multidimensional solid-state NMR spectroscopy of plant cell walls.  United States: N. p., 2016. 
        Web.  doi:10.1016/j.ssnmr.2016.08.001.

Copy to clipboard


                    Wang, Tuo, Phyo, Pyae, & Hong, Mei. Multidimensional solid-state NMR spectroscopy of plant cell walls.  United States.  doi:10.1016/j.ssnmr.2016.08.001.

Copy to clipboard


                    Wang, Tuo, Phyo, Pyae, and Hong, Mei. Thu .  
        "Multidimensional solid-state NMR spectroscopy of plant cell walls".  United States.  doi:10.1016/j.ssnmr.2016.08.001.  https://www.osti.gov/servlets/purl/1388014.

Copy to clipboard


                    
@article{osti_1388014,

  title        = {Multidimensional solid-state NMR spectroscopy of plant cell walls},

  author       = {Wang, Tuo and Phyo, Pyae and Hong, Mei},

  abstractNote = {Plant biomass has become an important source of bio-renewable energy in modern society. The molecular structure of plant cell walls is difficult to characterize by most atomic-resolution techniques due to the insoluble and disordered nature of the cell wall. Solid-state NMR (SSNMR) spectroscopy is uniquely suited for studying native hydrated plant cell walls at the molecular level with chemical resolution. Significant progress has been made in the last five years to elucidate the molecular structures and interactions of cellulose and matrix polysaccharides in plant cell walls. These studies have focused on primary cell walls of growing plants in both the dicotyledonous and grass families, as represented by the model plants Arabidopsis thaliana, Brachypodium distachyon, and Zea mays. To date, these SSNMR results have shown that 1) cellulose, hemicellulose, and pectins form a single network in the primary cell wall; 2) in dicot cell walls, the protein expansin targets the hemicellulose-enriched region of the cellulose microfibril for its wall-loosening function; and 3) primary wall cellulose has polymorphic structures that are distinct from the microbial cellulose structures. This article summarizes these key findings, and points out future directions of investigation to advance our fundamental understanding of plant cell wall structure and function.},

  doi          = {10.1016/j.ssnmr.2016.08.001},

  journal      = {Solid State Nuclear Magnetic Resonance},

  issn         = {0926-2040},

  number       = C,

  volume       = 78,

  place        = {United States},

  year         = {2016},

  month        = {9}

}

Copy to clipboard

Journal Article:

Free Publicly Available Full Text

Accepted Manuscript (Publisher)

Accepted Manuscript (DOE)

Publisher's Version of Record

DOI: 10.1016/j.ssnmr.2016.08.001

Other availability

Search WorldCat to find libraries that may hold this journal

Citation Metrics:

Cited by: 16 works

Citation information provided by
Web of Science

Save / Share:

Export Metadata

Save to My Library

Similar records in OSTI.GOV collections:

Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations

Journal Article Wang, Tuo ; Yang, Hui ; Kubicki, James D. ; ... - Biomacromolecules

The native cellulose of bacterial, algal, and animal origins has been well studied structurally using X-ray and neutron diffraction and solid-state NMR spectroscopy, and is known to consist of varying proportions of two allomorphs, Iα and Iβ, which differ in hydrogen bonding, chain packing, and local conformation. In comparison, cellulose structure in plant primary cell walls is much less understood because plant cellulose has lower crystallinity and extensive interactions with matrix polysaccharides. Here we have combined two-dimensional magic-angle-spinning (MAS) solid-state nuclear magnetic resonance (solid-state NMR) spectroscopy at high magnetic fields with density functional theory (DFT) calculations to obtain detailed informationmore »« less
Cited by 30
DOI: 10.1021/acs.biomac.6b00441

Full Text Available
Defining Determinants and Dynamics and Cellulose Microfibril Biosynthesis, Assembly and Degredation OSP Number: 63079/A001

Technical Report None, None

The central paradigm for converting plant biomass into soluble sugars for subsequent conversion to transportation fuels involves the enzymatic depolymerization of lignocellulosic plant cell walls by microbial enzymes. Despite decades of intensive research, this is still a relatively inefficient process, due largely to the recalcitrance and enormous complexity of the substrate. A major obstacle is still insufficient understanding of the detailed structure and biosynthesis of major wall components, including cellulose. For example, although cellulose is generally depicted as rigid, insoluble, uniformly crystalline microfibrils that are resistant to enzymatic degradation, the in vivo structures of plant cellulose microfibrils are surprisingly complex.more »« less
DOI: 10.2172/1361024

Full Text Available
Structure and Dynamics of Brachypodium Primary Cell Wall Polysaccharides from Two-Dimensional ¹³C Solid-State Nuclear Magnetic Resonance Spectroscopy

Journal Article Wang, Tuo ; Salazar, Andre ; Zabotina, Olga A. ; ... - Biochemistry

The polysaccharide structure and dynamics in the primary cell wall of the model grass Brachypodium distachyon are investigated for the first time using solid-state nuclear magnetic resonance (NMR). While both grass and non-grass cell walls contain cellulose as the main structural scaffold, the former contains xylan with arabinose and glucuronic acid substitutions as the main hemicellulose, with a small amount of xyloglucan (XyG) and pectins, while the latter contains XyG as the main hemicellulose and significant amounts of pectins. We labeled the Brachypodium cell wall with ¹³C to allow two-dimensional (2D) ¹³C correlation NMR experiments under magic-angle spinning. Well-resolved 2Dmore »« less
DOI: 10.1021/bi500231b
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls

Journal Article Wang, Tuo ; Park, Yong Bum ; Caporini, Marc A. ; ... - Proceedings of the National Academy of Sciences of the United States of America

Structure determination of protein binding to noncrystalline macromolecular assemblies such as plant cell walls (CWs) poses a significant structural biology challenge. CWs are loosened during growth by expansin proteins, which weaken the noncovalent network formed by cellulose, hemicellulose, and pectins, but the CW target of expansins has remained elusive because of the minute amount of the protein required for activity and the complex nature of the CW. Using solid-state NMR spectroscopy, combined with sensitivity-enhancing dynamic nuclear polarization (DNP) and differential isotopic labeling of expansin and polysaccharides, we have now determined the functional binding target of expansin in the Arabidopsis thalianamore »« less
DOI: 10.1073/pnas.1316290110
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls

Journal Article Wang, Tuo ; Park, Yong Bum ; Caporini, Marc A. ; ... - Proceedings of the National Academy of Sciences of the United States of America

Structure determination of protein binding to noncrystalline macromolecular assemblies such as plant cell walls (CWs) poses a significant structural biology challenge. CWs are loosened during growth by expansin proteins, which weaken the noncovalent network formed by cellulose, hemicellulose, and pectins, but the CW target of expansins has remained elusive because of the minute amount of the protein required for activity and the complex nature of the CW. Using solid-state NMR spectroscopy, combined with sensitivity-enhancing dynamic nuclear polarization (DNP) and differential isotopic labeling of expansin and polysaccharides, we have now determined the functional binding target of expansin in the Arabidopsis thalianamore »« less
DOI: 10.1073/pnas.1316290110

Similar Records