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Title: Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR

Abstract

Acidification of plant primary cell walls causes cell wall expansion and plant growth. To understand how acidic pH affects the molecular structure and dynamics of wall polysaccharides, we have now characterized and compared Arabidopsis thaliana primary cell walls in neutral (pH 6.8) and acidic (pH 4.0) conditions using solid-state NMR spectroscopy. Quantitative 13C solid-state NMR spectra indicate that the pH 4.0 cell wall has neutral galacturonic acid residues in homogalacturonan (HG) and rhamnogalacturonan (RG). 13C INEPT spectra, which selectively detect highly dynamic polymers, indicate that some of the HG and RG chains in the interfibrillar region have become more dynamic in the acidic wall compared to the neutral cell wall, whereas other chains have become more rigid. Consistent with this increased dynamic heterogeneity, C–H dipolar couplings and 2D 13C–13C correlation spectra indicate that some of the HG backbones are partially aggregated in the acidic cell wall. Moreover, 2D correlation spectra measured with long mixing times indicate that the acidic cell wall has weaker cellulose–pectin interactions, and water-polysaccharide 1H spin diffusion data show that cellulose microfibrils are better hydrated at low pH. Taken together, these results indicate a cascade of chemical and conformational changes of wall polysaccharides due to cell wallmore » acidification. These changes start with neutralization of the pectic polysaccharides, which disrupts calcium crosslinking of HG, causes partial aggregation of the interfibrillar HG, weakens cellulose–pectin interactions, and increases the hydration of both cellulose microfibrils and matrix polysaccharides. These molecular-level structural and dynamical changes are expected to facilitate polysaccharide slippage, which underlies cell wall loosening and expansion, and may occur both independent of and as a consequence of protein-mediated wall loosening.« less

Authors:
; ;
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) (SC-22)
OSTI Identifier:
1566415
DOE Contract Number:  
SC0001090
Resource Type:
Journal Article
Journal Name:
Cellulose
Additional Journal Information:
Journal Volume: 26; Journal Issue: 1; Journal ID: ISSN 0969-0239
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
biofuels (including algae and biomass), bio-inspired, membrane, carbon sequestration, materials and chemistry by design, synthesis (self-assembly)

Citation Formats

Phyo, Pyae, Gu, Ying, and Hong, Mei. Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR. United States: N. p., 2018. Web. doi:10.1007/s10570-018-2094-7.
Phyo, Pyae, Gu, Ying, & Hong, Mei. Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR. United States. doi:10.1007/s10570-018-2094-7.
Phyo, Pyae, Gu, Ying, and Hong, Mei. Wed . "Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR". United States. doi:10.1007/s10570-018-2094-7.
@article{osti_1566415,
title = {Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR},
author = {Phyo, Pyae and Gu, Ying and Hong, Mei},
abstractNote = {Acidification of plant primary cell walls causes cell wall expansion and plant growth. To understand how acidic pH affects the molecular structure and dynamics of wall polysaccharides, we have now characterized and compared Arabidopsis thaliana primary cell walls in neutral (pH 6.8) and acidic (pH 4.0) conditions using solid-state NMR spectroscopy. Quantitative 13C solid-state NMR spectra indicate that the pH 4.0 cell wall has neutral galacturonic acid residues in homogalacturonan (HG) and rhamnogalacturonan (RG). 13C INEPT spectra, which selectively detect highly dynamic polymers, indicate that some of the HG and RG chains in the interfibrillar region have become more dynamic in the acidic wall compared to the neutral cell wall, whereas other chains have become more rigid. Consistent with this increased dynamic heterogeneity, C–H dipolar couplings and 2D 13C–13C correlation spectra indicate that some of the HG backbones are partially aggregated in the acidic cell wall. Moreover, 2D correlation spectra measured with long mixing times indicate that the acidic cell wall has weaker cellulose–pectin interactions, and water-polysaccharide 1H spin diffusion data show that cellulose microfibrils are better hydrated at low pH. Taken together, these results indicate a cascade of chemical and conformational changes of wall polysaccharides due to cell wall acidification. These changes start with neutralization of the pectic polysaccharides, which disrupts calcium crosslinking of HG, causes partial aggregation of the interfibrillar HG, weakens cellulose–pectin interactions, and increases the hydration of both cellulose microfibrils and matrix polysaccharides. These molecular-level structural and dynamical changes are expected to facilitate polysaccharide slippage, which underlies cell wall loosening and expansion, and may occur both independent of and as a consequence of protein-mediated wall loosening.},
doi = {10.1007/s10570-018-2094-7},
journal = {Cellulose},
issn = {0969-0239},
number = 1,
volume = 26,
place = {United States},
year = {2018},
month = {10}
}

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