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Title: Grass xylan structural variation suggests functional specialization and distinctive interaction with cellulose and lignin

Abstract

SUMMARY Xylan is the most abundant non‐cellulosic polysaccharide in grass cell walls, and it has important structural roles. The name glucuronoarabinoxylan (GAX) is used to describe this variable hemicellulose. It has a linear backbone of β‐1,4‐xylose (Xyl) residues that may be substituted with α‐1,2‐linked (4‐ O ‐methyl)‐glucuronic acid (GlcA), α‐1,3‐linked arabinofuranose (Ara f ), and sometimes acetylation at the O ‐2 and/or O ‐3 positions. The role of these substitutions remains unclear, although there is increasing evidence that they affect the way xylan interacts with other cell wall components, particularly cellulose and lignin. Here, we used substitution‐dependent endo‐xylanase enzymes to investigate the variability of xylan substitution in grass culm cell walls. We show that there are at least three different types of xylan: (i) an arabinoxylan with evenly distributed Ara f substitutions without GlcA (AXe); (ii) a glucuronoarabinoxylan with clustered GlcA modifications (GAXc); and (iii) a highly substituted glucuronoarabinoxylan (hsGAX). Immunolocalization of AXe and GAXc in Brachypodium distachyon culms revealed that these xylan types are not restricted to a few cell types but are instead widely detected in Brachypodium cell walls. We hypothesize that there are functionally specialized xylan types within the grass cell wall. The even substitutions of AXemore » may permit folding and binding on the surface of cellulose fibrils, whereas the more complex substitutions of the other xylans may support a role in the matrix and interaction with other cell wall components.« less

Authors:
ORCiD logo [1];  [2];  [1];  [1]; ORCiD logo [3];  [1]; ORCiD logo [1]
  1. Department of Biochemistry, School of Biological Sciences University of Cambridge Cambridge CB2 1QW UK
  2. Sainsbury Laboratory University of Cambridge Cambridge CB2 1LR UK
  3. Department of Chemistry, School of Engineering Sciences in Chemistry, Biotechnology and Health KTH Royal Institute of Technology Stockholm SE‐10691 Sweden
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1909963
Alternate Identifier(s):
OSTI ID: 1909967; OSTI ID: 2204045
Grant/Contract Number:  
DE‐SC0001090; SC0001090
Resource Type:
Published Article
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Name: The Plant Journal Journal Volume: 113 Journal Issue: 5; Journal ID: ISSN 0960-7412
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; Miscanthus sinensis; Brachypodium distachyon; grass xylan; polysaccharide substitution patterns; grass cell wall; arabinosylation; glucuronidation; xylan–lignin interactions; xylan–cellulose interactions; cell wall molecular architecture

Citation Formats

Tryfona, Theodora, Bourdon, Matthieu, Delgado Marques, Rita, Busse‐Wicher, Marta, Vilaplana, Francisco, Stott, Katherine, and Dupree, Paul. Grass xylan structural variation suggests functional specialization and distinctive interaction with cellulose and lignin. United Kingdom: N. p., 2023. Web. doi:10.1111/tpj.16096.
Tryfona, Theodora, Bourdon, Matthieu, Delgado Marques, Rita, Busse‐Wicher, Marta, Vilaplana, Francisco, Stott, Katherine, & Dupree, Paul. Grass xylan structural variation suggests functional specialization and distinctive interaction with cellulose and lignin. United Kingdom. https://doi.org/10.1111/tpj.16096
Tryfona, Theodora, Bourdon, Matthieu, Delgado Marques, Rita, Busse‐Wicher, Marta, Vilaplana, Francisco, Stott, Katherine, and Dupree, Paul. Thu . "Grass xylan structural variation suggests functional specialization and distinctive interaction with cellulose and lignin". United Kingdom. https://doi.org/10.1111/tpj.16096.
@article{osti_1909963,
title = {Grass xylan structural variation suggests functional specialization and distinctive interaction with cellulose and lignin},
author = {Tryfona, Theodora and Bourdon, Matthieu and Delgado Marques, Rita and Busse‐Wicher, Marta and Vilaplana, Francisco and Stott, Katherine and Dupree, Paul},
abstractNote = {SUMMARY Xylan is the most abundant non‐cellulosic polysaccharide in grass cell walls, and it has important structural roles. The name glucuronoarabinoxylan (GAX) is used to describe this variable hemicellulose. It has a linear backbone of β‐1,4‐xylose (Xyl) residues that may be substituted with α‐1,2‐linked (4‐ O ‐methyl)‐glucuronic acid (GlcA), α‐1,3‐linked arabinofuranose (Ara f ), and sometimes acetylation at the O ‐2 and/or O ‐3 positions. The role of these substitutions remains unclear, although there is increasing evidence that they affect the way xylan interacts with other cell wall components, particularly cellulose and lignin. Here, we used substitution‐dependent endo‐xylanase enzymes to investigate the variability of xylan substitution in grass culm cell walls. We show that there are at least three different types of xylan: (i) an arabinoxylan with evenly distributed Ara f substitutions without GlcA (AXe); (ii) a glucuronoarabinoxylan with clustered GlcA modifications (GAXc); and (iii) a highly substituted glucuronoarabinoxylan (hsGAX). Immunolocalization of AXe and GAXc in Brachypodium distachyon culms revealed that these xylan types are not restricted to a few cell types but are instead widely detected in Brachypodium cell walls. We hypothesize that there are functionally specialized xylan types within the grass cell wall. The even substitutions of AXe may permit folding and binding on the surface of cellulose fibrils, whereas the more complex substitutions of the other xylans may support a role in the matrix and interaction with other cell wall components.},
doi = {10.1111/tpj.16096},
journal = {The Plant Journal},
number = 5,
volume = 113,
place = {United Kingdom},
year = {Thu Jan 19 00:00:00 EST 2023},
month = {Thu Jan 19 00:00:00 EST 2023}
}

Journal Article:
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https://doi.org/10.1111/tpj.16096

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