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Probing the molecular architecture of Arabidopsis thaliana secondary cell walls using two- and three-dimensional 13C solid state nuclear magnetic resonance spectroscopy
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Dupree, Ray, Simmons, Thomas J., Mortimer, Jennifer C., Patel, Dharmesh, Iuga, Dinu, Brown, Steven P. and Dupree, Paul (2015) Probing the molecular architecture of Arabidopsis thaliana secondary cell walls using two- and three-dimensional 13C solid state nuclear magnetic resonance spectroscopy. Biochemistry, Volume 54 (Number 14). pp. 2335-2345. doi:10.1021/bi501552k ISSN 0006-2960.
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Official URL: http://dx.doi.org/10.1021/bi501552k
Abstract
The plant secondary cell wall is a thickened polysaccharide and phenolic structure, providing mechanical strength to cells, particularly in woody tissues. It is the main feedstock for the developing bioenergy and green chemistry industries. Despite the role that molecular architecture (the arrangement of biopolymers relative to each other, and their conformations) plays in dictating biomass properties, such as recalcitrance to breakdown, it is poorly understood. Here, unprocessed dry 13C-labeled stems from the model plant Arabidopsis thaliana were analyzed by a variety of 13C solid state magic angle spinning nuclear magnetic resonance methods, such as one-dimensional cross-polarization and direct polarization, two-dimensional refocused INADEQUATE, RFDR, PDSD, and three-dimensional DARR, demonstrating their viability for the study of native polymer arrangements in intact secondary cell walls. All carbon sites of the two main glucose environments in cellulose (previously assigned to microfibril surface and interior residues) are clearly resolved, as are carbon sites of the other major components of the secondary cell wall: xylan and lignin. The xylan carbon 4 chemical shift is markedly different from that reported previously for solution or primary cell wall xylan, indicating significant changes in the helical conformation in these dried stems. Furthermore, the shift span indicates that xylan adopts a wide range of conformations in this material, with very little in the 31 conformation typical of xylan in solution. Additionally, spatial connections of noncarbohydrate species were observed with both cellulose peaks conventionally assigned as “surface” and as “interior” cellulose environments, raising questions about the origin of these two cellulose signals. In woody plant tissues, a secondary cell wall is laid down on the interior of the thin, extensible, and biochemically and functionally distinct primary cell wall during cellular differentiation. The secondary wall is crucial to many aspects of plant physiology, including mechanical strength. It also comprises the vast majority of the material of mature plant tissues and lignocellulosic biomass and is therefore an invaluable resource for renewable materials and for bioenergy feedstocks.1,2 The polysaccharide components of the cell wall, which constitute more than 60% of its dry weight, are commonly categorized into three constituent types: cellulose, hemicellulose, and pectin.3,4 Cellulose is thought to be the main load-bearing structure of the cell wall and is the most abundant polymer in both primary and secondary walls.5 Cellulose chains are composed of β-(1→4)-D-glucosyl residues (Figure 1) that are partly assembled into layers in a microfibril by inter- and intrachain hydrogen bonding and hydrophobic interactions. Within crystalline regions of cellulose microfibrils (known as crystallites), glucan chains are found in a 2-fold (21) helical conformation.
Item Type: | Journal Article | ||||||||
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Subjects: | Q Science > QC Physics Q Science > QD Chemistry Q Science > QK Botany |
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Divisions: | Faculty of Science, Engineering and Medicine > Science > Physics | ||||||||
Library of Congress Subject Headings (LCSH): | Plant cell walls, Nuclear magnetic resonance spectroscopy, Arabidopsis thaliana | ||||||||
Journal or Publication Title: | Biochemistry | ||||||||
Publisher: | American Chemical Society | ||||||||
ISSN: | 0006-2960 | ||||||||
Official Date: | 4 March 2015 | ||||||||
Dates: |
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Volume: | Volume 54 | ||||||||
Number: | Number 14 | ||||||||
Number of Pages: | 11 | ||||||||
Page Range: | pp. 2335-2345 | ||||||||
DOI: | 10.1021/bi501552k | ||||||||
Status: | Peer Reviewed | ||||||||
Publication Status: | Published | ||||||||
Access rights to Published version: | Open Access (Creative Commons) | ||||||||
Copyright Holders: | ACS | ||||||||
Date of first compliant deposit: | 29 December 2015 | ||||||||
Date of first compliant Open Access: | 29 December 2015 | ||||||||
Funder: | Biotechnology and Biological Sciences Research Council (Great Britain) (BBSRC), Engineering and Physical Sciences Research Council (EPSRC), Advantage West Midlands (AWM), Birmingham Science City, European Regional Development Fund (ERDF) | ||||||||
Grant number: | BB/G016240/1 (BBSRC), EP/F017901/1 (EPSRC) |
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