An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls

International audience 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...

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Published in:Nature Plants
Main Authors: Grantham, Nicholas J., Wurman-Rodrich, Joel, Terrett, Oliver M., Lyczakowski, Jan J., Stott, Katherine, Iuga, Dinu, Simmons, Thomas J., Durand Tardif, Mylène, Brown, Steven. P., Dupree, Ray, Busse-Wicher, Marta, Dupree, Paul
Other Authors: Department of Biochemistry, University of Cambridge UK (CAM), University of Warwick, Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Centre National de la Recherche Scientifique (CNRS), Université Paris Saclay (COmUE), Leverhulme Trust, Conicyt Chile, Cambridge Trusts, BBSRC BB/J014540/1, PR140003, BBSRC Novozymes iCASE award BB/M015432/1, EPSRC, University of Warwick through Advantage West Midlands (AWM), European Regional Development Fund (ERDF)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2017
Subjects:
Online Access:https://hal.inrae.fr/hal-02629187
https://doi.org/10.1038/s41477-017-0030-8
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spelling ftunivnantes:oai:HAL:hal-02629187v1 2023-05-15T16:07:28+02:00 An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, Nicholas J. Wurman-Rodrich, Joel Terrett, Oliver M. Lyczakowski, Jan J. Stott, Katherine Iuga, Dinu Simmons, Thomas J. Durand Tardif, Mylène Brown, Steven. P. Dupree, Ray Busse-Wicher, Marta Dupree, Paul Department of Biochemistry University of Cambridge UK (CAM) University of Warwick Institut Jean-Pierre Bourgin (IJPB) Institut National de la Recherche Agronomique (INRA)-AgroParisTech Centre National de la Recherche Scientifique (CNRS) Université Paris Saclay (COmUE) Leverhulme Trust Conicyt Chile Cambridge Trusts BBSRC BB/J014540/1, PR140003 BBSRC Novozymes iCASE award BB/M015432/1 EPSRC University of Warwick through Advantage West Midlands (AWM) European Regional Development Fund (ERDF) 2017 https://hal.inrae.fr/hal-02629187 https://doi.org/10.1038/s41477-017-0030-8 en eng HAL CCSD Nature Publishing Group info:eu-repo/semantics/altIdentifier/doi/10.1038/s41477-017-0030-8 info:eu-repo/semantics/altIdentifier/pmid/28993612 hal-02629187 https://hal.inrae.fr/hal-02629187 doi:10.1038/s41477-017-0030-8 PRODINRA: 421582 PUBMED: 28993612 WOS: 000414512800011 ISSN: 2055-026X EISSN: 2055-0278 Nature Plants https://hal.inrae.fr/hal-02629187 Nature Plants, Nature Publishing Group, 2017, 3 (11), pp.859-865. ⟨10.1038/s41477-017-0030-8⟩ https://www.nature.com/nplants/ [SDV.BV]Life Sciences [q-bio]/Vegetal Biology info:eu-repo/semantics/article Journal articles 2017 ftunivnantes https://doi.org/10.1038/s41477-017-0030-8 2022-08-10T04:05:44Z International audience 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(1-3). Consequently, xylan adopts a flattened ribbon-like twofold screw conformation when bound to cellulose in the cell wall(4). 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 enables the interaction of xylan with hydrophilic faces of cellulose fibrils, and is essential for development of normal plant secondary cell walls. Article in Journal/Newspaper eskimo* Université de Nantes: HAL-UNIV-NANTES Nature Plants 3 11 859 865
institution Open Polar
collection Université de Nantes: HAL-UNIV-NANTES
op_collection_id ftunivnantes
language English
topic [SDV.BV]Life Sciences [q-bio]/Vegetal Biology
spellingShingle [SDV.BV]Life Sciences [q-bio]/Vegetal Biology
Grantham, Nicholas J.
Wurman-Rodrich, Joel
Terrett, Oliver M.
Lyczakowski, Jan J.
Stott, Katherine
Iuga, Dinu
Simmons, Thomas J.
Durand Tardif, Mylène
Brown, Steven. P.
Dupree, Ray
Busse-Wicher, Marta
Dupree, Paul
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls
topic_facet [SDV.BV]Life Sciences [q-bio]/Vegetal Biology
description International audience 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(1-3). Consequently, xylan adopts a flattened ribbon-like twofold screw conformation when bound to cellulose in the cell wall(4). 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 enables the interaction of xylan with hydrophilic faces of cellulose fibrils, and is essential for development of normal plant secondary cell walls.
author2 Department of Biochemistry
University of Cambridge UK (CAM)
University of Warwick
Institut Jean-Pierre Bourgin (IJPB)
Institut National de la Recherche Agronomique (INRA)-AgroParisTech
Centre National de la Recherche Scientifique (CNRS)
Université Paris Saclay (COmUE)
Leverhulme Trust
Conicyt Chile
Cambridge Trusts
BBSRC BB/J014540/1, PR140003
BBSRC Novozymes iCASE award BB/M015432/1
EPSRC
University of Warwick through Advantage West Midlands (AWM)
European Regional Development Fund (ERDF)
format Article in Journal/Newspaper
author Grantham, Nicholas J.
Wurman-Rodrich, Joel
Terrett, Oliver M.
Lyczakowski, Jan J.
Stott, Katherine
Iuga, Dinu
Simmons, Thomas J.
Durand Tardif, Mylène
Brown, Steven. P.
Dupree, Ray
Busse-Wicher, Marta
Dupree, Paul
author_facet Grantham, Nicholas J.
Wurman-Rodrich, Joel
Terrett, Oliver M.
Lyczakowski, Jan J.
Stott, Katherine
Iuga, Dinu
Simmons, Thomas J.
Durand Tardif, Mylène
Brown, Steven. P.
Dupree, Ray
Busse-Wicher, Marta
Dupree, Paul
author_sort Grantham, Nicholas J.
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 HAL CCSD
publishDate 2017
url https://hal.inrae.fr/hal-02629187
https://doi.org/10.1038/s41477-017-0030-8
genre eskimo*
genre_facet eskimo*
op_source ISSN: 2055-026X
EISSN: 2055-0278
Nature Plants
https://hal.inrae.fr/hal-02629187
Nature Plants, Nature Publishing Group, 2017, 3 (11), pp.859-865. ⟨10.1038/s41477-017-0030-8⟩
https://www.nature.com/nplants/
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1038/s41477-017-0030-8
info:eu-repo/semantics/altIdentifier/pmid/28993612
hal-02629187
https://hal.inrae.fr/hal-02629187
doi:10.1038/s41477-017-0030-8
PRODINRA: 421582
PUBMED: 28993612
WOS: 000414512800011
op_doi https://doi.org/10.1038/s41477-017-0030-8
container_title Nature Plants
container_volume 3
container_issue 11
container_start_page 859
op_container_end_page 865
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