skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14

Abstract

Xylan is a crucial component of many plant primary and secondary cell walls. However, the structure and function of xylan in the dicotyledon primary cell wall is not well understood. Here, we characterized a xylan that is specific to tissues enriched in Arabidopsis primary cell walls. Unlike previously described xylans, this xylan carries a pentose linked 1–2 to the α-1,2-d-glucuronic acid (GlcA) side chains on the β-1,4-Xyl backbone. The frequent and precisely regular spacing of GlcA substitutions every six xylosyl residues along the backbone is also unlike that previously observed in secondary cell wall xylan. Molecular genetics, in vitro assays, and expression data suggest that IRX9L, IRX10L and IRX14 are required for xylan backbone synthesis in primary cell wall synthesising tissues. IRX9 and IRX10 are not involved in the primary cell wall xylan synthesis but are functionally exchangeable with IRX9L and IRX10L. GUX3 is the only glucuronyltransferase required for the addition of the GlcA decorations on the xylan. Lastly, the differences in xylan structure in primary versus secondary cell walls might reflect the different roles in cross-linking and interaction with other cell wall components.

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2]
  1. Univ. of Cambridge, Cambridge (United Kingdom). Dept. of Biochemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Div.
  2. Univ. of Cambridge, Cambridge (United Kingdom). Dept. of Biochemistry.
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1213058
Alternate Identifier(s):
OSTI ID: 1407271
Grant/Contract Number:
AC02-05CH11231; BB/G016240/1; 251132; BB/K005537/1
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Journal Volume: 83; Journal Issue: 3; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Xylan; IRX10L; IRX9L; IRX14; GUX3; primary wall; Arabidopsis thaliana

Citation Formats

Mortimer, Jenny C., Faria-Blanc, Nuno, Yu, Xiaolan, Tryfona, Theodora, Sorieul, Mathias, Ng, Yao Z., Zhang, Zhinong, Stott, Katherine, Anders, Nadine, and Dupree, Paul. An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. United States: N. p., 2015. Web. doi:10.1111/tpj.12898.
Mortimer, Jenny C., Faria-Blanc, Nuno, Yu, Xiaolan, Tryfona, Theodora, Sorieul, Mathias, Ng, Yao Z., Zhang, Zhinong, Stott, Katherine, Anders, Nadine, & Dupree, Paul. An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. United States. doi:10.1111/tpj.12898.
Mortimer, Jenny C., Faria-Blanc, Nuno, Yu, Xiaolan, Tryfona, Theodora, Sorieul, Mathias, Ng, Yao Z., Zhang, Zhinong, Stott, Katherine, Anders, Nadine, and Dupree, Paul. Thu . "An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14". United States. doi:10.1111/tpj.12898. https://www.osti.gov/servlets/purl/1213058.
@article{osti_1213058,
title = {An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14},
author = {Mortimer, Jenny C. and Faria-Blanc, Nuno and Yu, Xiaolan and Tryfona, Theodora and Sorieul, Mathias and Ng, Yao Z. and Zhang, Zhinong and Stott, Katherine and Anders, Nadine and Dupree, Paul},
abstractNote = {Xylan is a crucial component of many plant primary and secondary cell walls. However, the structure and function of xylan in the dicotyledon primary cell wall is not well understood. Here, we characterized a xylan that is specific to tissues enriched in Arabidopsis primary cell walls. Unlike previously described xylans, this xylan carries a pentose linked 1–2 to the α-1,2-d-glucuronic acid (GlcA) side chains on the β-1,4-Xyl backbone. The frequent and precisely regular spacing of GlcA substitutions every six xylosyl residues along the backbone is also unlike that previously observed in secondary cell wall xylan. Molecular genetics, in vitro assays, and expression data suggest that IRX9L, IRX10L and IRX14 are required for xylan backbone synthesis in primary cell wall synthesising tissues. IRX9 and IRX10 are not involved in the primary cell wall xylan synthesis but are functionally exchangeable with IRX9L and IRX10L. GUX3 is the only glucuronyltransferase required for the addition of the GlcA decorations on the xylan. Lastly, the differences in xylan structure in primary versus secondary cell walls might reflect the different roles in cross-linking and interaction with other cell wall components.},
doi = {10.1111/tpj.12898},
journal = {The Plant Journal},
number = 3,
volume = 83,
place = {United States},
year = {Thu Jun 04 00:00:00 EDT 2015},
month = {Thu Jun 04 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 27works
Citation information provided by
Web of Science

Save / Share:
  • Xylan is a crucial component of many plant primary and secondary cell walls. However, the structure and function of xylan in the dicotyledon primary cell wall is not well understood. Here, we characterized a xylan that is specific to tissues enriched in Arabidopsis primary cell walls. Unlike previously described xylans, this xylan carries a pentose linked 1-2 to the α-1,2-d-glucuronic acid (GlcA) side chains on the β-1,4-Xyl backbone. The frequent and precisely regular spacing of GlcA substitutions every six xylosyl residues along the backbone is also unlike that previously observed in secondary cell wall xylan. Molecular genetics, in vitro assays,more » and expression data suggest that IRX9L, IRX10L and IRX14 are required for xylan backbone synthesis in primary cell wall synthesising tissues. IRX9 and IRX10 are not involved in the primary cell wall xylan synthesis but are functionally exchangeable with IRX9L and IRX10L. GUX3 is the only glucuronyltransferase required for the addition of the GlcA decorations on the xylan. The differences in xylan structure in primary versus secondary cell walls might reflect the different roles in cross-linking and interaction with other cell wall components. Significance Statement We have characterised a previously unreported type of xylan, which is a hemicellulose, in the Arabidopsis primary cell wall and shown that GUX3 is specifically responsible for adding the GlcA side chains with a precise spacing pattern. In addition, we have shown that only a subset of the known proteins responsible for xylan backbone elongation, IRX9L, IRX10L and IRX14, are necessary to synthesise this xylan.« less
  • Plant cell wall (CW) polysaccharides are responsible for the mechanical strength and growth of plant cells; however, the high-resolution structure and dynamics of the CW polysaccharides are still poorly understood because of the insoluble nature of these molecules. Here, we use 2D and 3D magic-angle-spinning (MAS) solid-state NMR (SSNMR) to investigate the structural role of pectins in the plant CW. Intact and partially depectinated primary CWs of Arabidopsis thaliana were uniformly labeled with 13C and their NMR spectra were compared. Recent 13C resonance assignment of the major polysaccharides in Arabidopsis thaliana CWs allowed us to determine the effects of depectinationmore » on the intermolecular packing and dynamics of the remaining wall polysaccharides. 2D and 3D correlation spectra show the suppression of pectin signals, confirming partial pectin removal by chelating agents and sodium carbonate. Importantly, higher cross peaks are observed in 2D and 3D 13C spectra of the depectinated CW, suggesting higher rigidity and denser packing of the remaining wall polysaccharides compared with the intact CW. 13C spin–lattice relaxation times and 1H rotating-frame spin–lattice relaxation times indicate that the polysaccharides are more rigid on both the nanosecond and microsecond timescales in the depectinated CW. Taken together, these results indicate that pectic polysaccharides are highly dynamic and endow the polysaccharide network of the primary CW with mobility and flexibility, which may be important for pectin functions. This study demonstrates the capability of multidimensional SSNMR to determine the intermolecular interactions and dynamic structures of complex plant materials under near-native conditions. Copyright © 2012 John Wiley & Sons, Ltd.« less