Water–Polysaccharide Interactions in the Primary Cell Wall of Arabidopsis thaliana from Polarization Transfer Solid-State NMR
Authors:
- 1 July 2014
- journal article
- research article
- Published by American Chemical Society (ACS) in Journal of the American Chemical Society
- Vol. 136 (29) , 10399-10409
Abstract
Polysaccharide-rich plant cell walls are hydrated under functional conditions, but the molecular interactions between water and polysaccharides in the wall have not been investigated. In this work, we employ polarization transfer solid-state NMR techniques to study the hydration of primary-wall polysaccharides of the model plant, Arabidopsis thaliana. By transferring water 1H polarization to polysaccharides through distance- and mobility-dependent 1H–1H dipolar couplings and detecting it through polysaccharide 13C signals, we obtain information about water proximity to cellulose, hemicellulose, and pectins as well as water mobility. Both intact and partially extracted cell wall samples are studied. Our results show that water–pectin polarization transfer is much faster than water–cellulose polarization transfer in all samples, but the extent of extraction has a profound impact on the water–polysaccharide spin diffusion. Removal of calcium ions and the consequent extraction of homogalacturonan (HG) significantly slowed down spin diffusion, while further extraction of matrix polysaccharides restored the spin diffusion rate. These trends are observed in cell walls with similar water content, thus they reflect inherent differences in the mobility and spatial distribution of water. Combined with quantitative analysis of the polysaccharide contents, our results indicate that calcium ions and HG gelation increase the amount of bound water, which facilitates spin diffusion, while calcium removal disrupts the gel and gives rise to highly dynamic water, which slows down spin diffusion. The recovery of spin diffusion rates after more extensive extraction is attributed to increased water-exposed surface areas of the polysaccharides. Water–pectin spin diffusion precedes water–cellulose spin diffusion, lending support to the single-network model of plant primary walls in which a substantial fraction of the cellulose surface is surrounded by pectins.Keywords
Funding Information
- Basic Energy Sciences (DE-AC02-07CH11358, DE-FG02-84ER13179, DE-SC0001090)
This publication has 53 references indexed in Scilit:
- A Revised Architecture of Primary Cell Walls Based on Biomechanical Changes Induced by Substrate-Specific EndoglucanasesPlant Physiology, 2012
- Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performanceBiotechnology for Biofuels, 2010
- Water−Protein Interactions of an Arginine-Rich Membrane Peptide in Lipid Bilayers Investigated by Solid-State Nuclear Magnetic Resonance SpectroscopyThe Journal of Physical Chemistry B, 2010
- Conformational Changes of an Ion Channel Detected Through Water−Protein Interactions Using Solid-State NMR SpectroscopyJournal of the American Chemical Society, 2010
- Observation of exchange of micropore water in cement pastes by two-dimensionalnuclear magnetic resonance relaxometryPhysical Review E, 2006
- Solid-state 13C-NMR spectroscopy shows that the xyloglucans in the primary cell walls of mung bean (Vigna radiata L.) occur in different domains: a new model for xyloglucan-cellulose interactions in the cell wallJournal of Experimental Botany, 2004
- A New NMR Method for the Study of Local Mobility in Solids and Application to Hydration of Biopolymers in Plant Cell WallsMacromolecules, 2002
- 2D and 3D15N−13C−13C NMR Chemical Shift Correlation Spectroscopy of Solids: Assignment of MAS Spectra of PeptidesJournal of the American Chemical Society, 2000
- Determination of Through-Bond Carbon−Carbon Connectivities in Solid-State NMR Using the INADEQUATE ExperimentJournal of the American Chemical Society, 1997
- Chemistry and uses of pectin — A reviewCritical Reviews in Food Science and Nutrition, 1997