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Title: Direct Determination of Hydroxymethyl Conformations of Plant Cell Wall Cellulose Using 1H Polarization Transfer Solid-State NMR

Journal Article · · Biomacromolecules
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Chemistry
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Structural Molecular Biology
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In contrast to the well-studied crystalline cellulose of microbial and animal origins, cellulose in plant cell walls is disordered due to its interactions with matrix polysaccharides. Plant cell wall (PCW) is an undisputed source of sustainable global energy; therefore, it is important to determine the molecular structure of PCW cellulose. The most reactive component of cellulose is the exocyclic hydroxymethyl group: when it adopts the tg conformation, it stabilizes intrachain and interchain hydrogen bonding, while gt and gg conformations destabilize the hydrogen-bonding network. So far, information about the hydroxymethyl conformation in cellulose has been exclusively obtained from 13C chemical shifts of monosaccharides and oligosaccharides, which do not reflect the environment of cellulose in plant cell walls. Here, we use solid-state Nuclear Magnetic Resonance (ssNMR) spectroscopy to measure the hydroxymethyl torsion angle of cellulose in two model plants, by detecting distance-dependent polarization transfer between H4 and H6 protons in 2D 13C–13C correlation spectra. We show that the interior crystalline portion of cellulose microfibrils in Brachypodium and Arabidopsis cell walls exhibits H4–H6 polarization transfer curves that are indicative of a tg conformation, whereas surface cellulose chains exhibit slower H4–H6 polarization transfer that is best fit to the gt conformation. Joint constraints by the H4–H6 polarization transfer curves and 13C chemical shifts indicate that it is unlikely for interior cellulose to have a significant population of the gt and gg conformation mixed with the tg conformation, while surface cellulose may adopt a small percentage of the gg conformation. These results provide new constraints to the structure and matrix interactions of cellulose in plant cell walls, and represent the first direct determination of a torsion angle in an important noncrystalline carbohydrate polymer.

Research Organization:
Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
SC0001090
OSTI ID:
1470519
Journal Information:
Biomacromolecules, Vol. 19, Issue 5; Related Information: CLSF partners with Pennsylvania State University (lead); North Carolina State University; University of Rhode Island; Virginia Tech University; ISSN 1525-7797
Publisher:
American Chemical SocietyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 32 works
Citation information provided by
Web of Science

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Cited By (12)

Molecular-level driving forces in lignocellulosic biomass deconstruction for bioenergy journal October 2018
The molecular structure of plant sporopollenin journal December 2018
Solid-state NMR characterization of triacylglycerol and polysaccharides in coffee beans journal January 2019
Longitudinal Relaxation Optimization Enhances 1 H‐Detected HSQC in Solid‐State NMR Spectroscopy on Challenging Biological Systems journal February 2019
Molecular architecture of softwood revealed by solid-state NMR journal October 2019
Effects of ball milling on the structure of cotton cellulose journal January 2019
A density functional theory study on the shape of the primary cellulose microfibril in plants: effects of C6 exocyclic group conformation and H-bonding journal January 2020
Atomic resolution of cotton cellulose structure enabled by dynamic nuclear polarization solid-state NMR journal November 2018
Molecular architecture of softwood revealed by solid-state NMR. text January 2019
Solid-state NMR characterization of triacylglycerol and polysaccharides in coffee beans text January 2019
Solid-state NMR characterization of triacylglycerol and polysaccharides in coffee beans text January 2019
Molecular architecture of softwood revealed by solid-state NMR text January 2019

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