An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls
Xylan and cellulose are abundant polysaccharides in vascular plants and essential for secondary cell wall strength. Acetate or glucuronic acid decorations are exclusively found on even-numbered residues in most of the glucuronoxylan polymer. It has been proposed that this even-specific positioning o...
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ftunivcam:oai:www.repository.cam.ac.uk:1810/267933 2024-01-14T10:06:37+01:00 An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, NJ Wurman-Rodrich, J Terrett, OM Lyczakowski, JJ Stott, K Iuga, D Simmons, TJ Durand-Tardif, M Brown, SP Dupree, R Busse-Wicher, M Dupree, P 2017-11 application/pdf https://www.repository.cam.ac.uk/handle/1810/267933 https://doi.org/10.17863/CAM.13865 eng eng Nature Publishing Group http://dx.doi.org/10.1038/s41477-017-0030-8 Nature Plants https://doi.org/10.17863/CAM.12996 https://www.repository.cam.ac.uk/handle/1810/267933 doi:10.17863/CAM.13865 Biofuels Cell biology Cell wall Plant physiology Article 2017 ftunivcam https://doi.org/10.17863/CAM.1386510.17863/CAM.12996 2023-12-21T23:26:39Z Xylan and cellulose are abundant polysaccharides in vascular plants and essential for secondary cell wall strength. Acetate or glucuronic acid decorations are exclusively found on even-numbered residues in most of the glucuronoxylan polymer. It has been proposed that this even-specific positioning of the decorations might permit docking of xylan onto the hydrophilic face of a cellulose microfibril. Consequently, xylan adopts a flattened ribbon-like twofold helical screw conformation when bound to cellulose in the cell wall. Here we show that ESKIMO1/XOAT1/TBL29, a xylan-specific O-acetyltransferase, is necessary for generation of the even pattern of acetyl esters on xylan in Arabidopsis. The reduced acetylation in the esk1 mutant deregulates the position-specific activity of the xylan glucuronosyltransferase GUX1, and so the even pattern of glucuronic acid on the xylan is lost. Solid-state NMR of intact cell walls shows that, without the even-patterned xylan decorations, xylan does not interact normally with cellulose fibrils. We conclude that the even pattern of xylan substitutions seen across vascular plants therefore enables the interaction of xylan with hydrophilic faces of cellulose fibrils, and is essential for development of normal plant secondary cell walls. This work was part supported by the Leverhulme Trust grant for the Centre for Natural Material Innovation. J.W.-R., J.J.L. and O.M.T. are supported by studentships from Conicyt Chile and the Cambridge Trusts, the BBSRC Doctoral Training Partnership BB/J014540/1, and a BBSRC Novozymes iCASE award (BB/M015432/1) respectively. We thank K. B. Krogh for co-supervision of O.M.T. The UK 850 MHz solid-state NMR Facility used in this research was funded by EPSRC and BBSRC (Contract reference PR140003), as well as the University of Warwick including via part funding through Birmingham Science City Advanced Materials Projects 1 and 2 supported by Advantage West Midlands (AWM) and the European Regional Development Fund (ERDF). Article in Journal/Newspaper eskimo* Apollo - University of Cambridge Repository Krogh ENVELOPE(-66.984,-66.984,-66.275,-66.275) |
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Open Polar |
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Apollo - University of Cambridge Repository |
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ftunivcam |
language |
English |
topic |
Biofuels Cell biology Cell wall Plant physiology |
spellingShingle |
Biofuels Cell biology Cell wall Plant physiology Grantham, NJ Wurman-Rodrich, J Terrett, OM Lyczakowski, JJ Stott, K Iuga, D Simmons, TJ Durand-Tardif, M Brown, SP Dupree, R Busse-Wicher, M Dupree, P An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
topic_facet |
Biofuels Cell biology Cell wall Plant physiology |
description |
Xylan and cellulose are abundant polysaccharides in vascular plants and essential for secondary cell wall strength. Acetate or glucuronic acid decorations are exclusively found on even-numbered residues in most of the glucuronoxylan polymer. It has been proposed that this even-specific positioning of the decorations might permit docking of xylan onto the hydrophilic face of a cellulose microfibril. Consequently, xylan adopts a flattened ribbon-like twofold helical screw conformation when bound to cellulose in the cell wall. Here we show that ESKIMO1/XOAT1/TBL29, a xylan-specific O-acetyltransferase, is necessary for generation of the even pattern of acetyl esters on xylan in Arabidopsis. The reduced acetylation in the esk1 mutant deregulates the position-specific activity of the xylan glucuronosyltransferase GUX1, and so the even pattern of glucuronic acid on the xylan is lost. Solid-state NMR of intact cell walls shows that, without the even-patterned xylan decorations, xylan does not interact normally with cellulose fibrils. We conclude that the even pattern of xylan substitutions seen across vascular plants therefore enables the interaction of xylan with hydrophilic faces of cellulose fibrils, and is essential for development of normal plant secondary cell walls. This work was part supported by the Leverhulme Trust grant for the Centre for Natural Material Innovation. J.W.-R., J.J.L. and O.M.T. are supported by studentships from Conicyt Chile and the Cambridge Trusts, the BBSRC Doctoral Training Partnership BB/J014540/1, and a BBSRC Novozymes iCASE award (BB/M015432/1) respectively. We thank K. B. Krogh for co-supervision of O.M.T. The UK 850 MHz solid-state NMR Facility used in this research was funded by EPSRC and BBSRC (Contract reference PR140003), as well as the University of Warwick including via part funding through Birmingham Science City Advanced Materials Projects 1 and 2 supported by Advantage West Midlands (AWM) and the European Regional Development Fund (ERDF). |
format |
Article in Journal/Newspaper |
author |
Grantham, NJ Wurman-Rodrich, J Terrett, OM Lyczakowski, JJ Stott, K Iuga, D Simmons, TJ Durand-Tardif, M Brown, SP Dupree, R Busse-Wicher, M Dupree, P |
author_facet |
Grantham, NJ Wurman-Rodrich, J Terrett, OM Lyczakowski, JJ Stott, K Iuga, D Simmons, TJ Durand-Tardif, M Brown, SP Dupree, R Busse-Wicher, M Dupree, P |
author_sort |
Grantham, NJ |
title |
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
title_short |
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
title_full |
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
title_fullStr |
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
title_full_unstemmed |
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
title_sort |
even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls |
publisher |
Nature Publishing Group |
publishDate |
2017 |
url |
https://www.repository.cam.ac.uk/handle/1810/267933 https://doi.org/10.17863/CAM.13865 |
long_lat |
ENVELOPE(-66.984,-66.984,-66.275,-66.275) |
geographic |
Krogh |
geographic_facet |
Krogh |
genre |
eskimo* |
genre_facet |
eskimo* |
op_relation |
https://doi.org/10.17863/CAM.12996 https://www.repository.cam.ac.uk/handle/1810/267933 doi:10.17863/CAM.13865 |
op_doi |
https://doi.org/10.17863/CAM.1386510.17863/CAM.12996 |
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1788061065055043584 |