These authors contributed equally to this work.
The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana
Article first published online: 15 JUL 2014
© 2014 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
The Plant Journal
Volume 79, Issue 3, pages 492–506, August 2014
How to Cite
Busse-Wicher, M., Gomes, T. C. F., Tryfona, T., Nikolovski, N., Stott, K., Grantham, N. J., Bolam, D. N., Skaf, M. S. and Dupree, P. (2014), The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a twofold helical screw in the secondary plant cell wall of Arabidopsis thaliana. The Plant Journal, 79: 492–506. doi: 10.1111/tpj.12575
- Issue published online: 24 JUL 2014
- Article first published online: 15 JUL 2014
- Accepted manuscript online: 2 JUN 2014 06:11AM EST
- Manuscript Accepted: 27 MAY 2014
- Manuscript Revised: 16 MAY 2014
- Manuscript Received: 19 APR 2014
- BBSRC Sustainable Energy Centre Cell Wall Sugars Programme (BSBEC). Grant Number: BB/G016240/1
- European Community's Seventh Framework Programme SUNLIBB. Grant Number: 251132
- Wellcome Trust
- CNPq. Grant Number: 140978/2009-7
- CEPROBIO. Grant Number: 490022/2009-0
- FAPESP. Grant Number: 2013/08293-7
- plant cell wall molecular architecture;
- cellulose interaction;
- Arabidopsis thaliana
The interaction between xylan and cellulose microfibrils is important for secondary cell wall properties in vascular plants; however, the molecular arrangement of xylan in the cell wall and the nature of the molecular bonding between the polysaccharides are unknown. In dicots, the xylan backbone of β-(1,4)-linked xylosyl residues is decorated by occasional glucuronic acid, and approximately one-half of the xylosyl residues are O-acetylated at C-2 or C-3. We recently proposed that the even, periodic spacing of GlcA residues in the major domain of dicot xylan might allow the xylan backbone to fold as a twofold helical screw to facilitate alignment along, and stable interaction with, cellulose fibrils; however, such an interaction might be adversely impacted by random acetylation of the xylan backbone. Here, we investigated the arrangement of acetyl residues in Arabidopsis xylan using mass spectrometry and NMR. Alternate xylosyl residues along the backbone are acetylated. Using molecular dynamics simulation, we found that a twofold helical screw conformation of xylan is stable in interactions with both hydrophilic and hydrophobic cellulose faces. Tight docking of xylan on the hydrophilic faces is feasible only for xylan decorated on alternate residues and folded as a twofold helical screw. The findings suggest an explanation for the importance of acetylation for xylan–cellulose interactions, and also have implications for our understanding of cell wall molecular architecture and properties, and biological degradation by pathogens and fungi. They will also impact strategies to improve lignocellulose processing for biorefining and bioenergy.