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 microfibril1,2,3. Consequently, xylan adopts a flattened ribbon-like twofold screw conformation when bound to cellulose in the cell wall4. 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.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $5.42 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Bromley, J. R. et al. GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 74, 423–434 (2013).
Busse-Wicher, M. et al. 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. Plant J. 79, 492–506 (2014).
Busse-Wicher, M. et al. Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose. Plant Physiol. 171, 2418–2431 (2016).
Simmons, T. J. et al. Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat. Commun. 7, 13902 (2016).
Scheller, H. V. & Ulvskov, P. Hemicelluloses. Annu. Rev. Plant Biol. 61, 263–289 (2010).
Kumar, M., Campbell, L. & Turner, S. Secondary cell walls: biosynthesis and manipulation. J. Exp. Bot. 67, 515–531 (2016).
Cosgrove, D. J. & Jarvis, M. C. Comparative structure and biomechanics of plant primary and secondary cell walls. Front. Plant Sci. 3, 204 (2012).
Fernandes, A. N. et al. Nanostructure of cellulose microfibrils in spruce wood. Proc. Natl Acad. Sci. USA 108, E1195–E1203 (2011).
Thomas, L. H. et al. Diffraction evidence for the structure of cellulose microfibrils in bamboo, a model for grass and cereal celluloses.BMC Plant Biol. 15, 153 (2015).
Wang, T. & Hong, M. Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J. Exp. Bot. 67, 503–514 (2016).
Ebringerová, A. & Heinze, T. Xylan and xylan derivatives—biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol. Rapid Commun. 21, 542–556 (2000).
Nieduszynski, I. A. & Marchessault, R. H. Structure of β-D-(1→4′)-xylan hydrate. Biopolymers 11, 1335–1344 (1972).
Li, L., Pérré, P., Frank, X. & Mazeau, K. A coarse-grain force-field for xylan and its interaction with cellulose. Carbohydr. Polym. 127, 438–450 (2015).
Pereira, C. S., Silveira, R. L., Dupree, P. & Skaf, M. S. Effects of xylan side-chain substitutions on xylan-cellulose interactions and implications for thermal pretreatment of cellulosic biomass. Biomacromolecules 18, 1311–1321 (2017).
Kabel, M. A., De Waard, P., Schols, H. A. & Voragen, A. G. J. Location of O-acetyl substituents in xylo-oligosaccharides obtained from hydrothermally treated Eucalyptus wood. Carbohydr. Res. 338, 69–77 (2003).
Mortimer, J. C. et al. Absence of branches from xylan in Arabidopsis gux mutants reveals potential for simplification of lignocellulosic biomass. Proc. Natl Acad. Sci. USA 107, 17409–17414 (2010).
Oikawa, A. et al. An integrative approach to the identification of Arabidopsis and rice genes involved in xylan and secondary wall development.PLoS ONE 5, e15481 (2010).
Urbanowicz, B. R. et al. 4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein. Proc. Natl Acad. Sci.USA 109, 14253–14258 (2012).
Rennie, E. A. et al. Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 159, 1408–1417 (2012).
Pawar, P. M.-A., Koutaniemi, S., Tenkanen, M. & Mellerowicz, E. J. Acetylation of woody lignocellulose: significance and regulation. Front. Plant Sci. 4, 118 (2013).
Busse-Wicher, M., Grantham, N. J., Lyczakowski, J. J., Nikolovski, N. & Dupree, P. Xylan decoration patterns and the plant secondary cell wall molecular architecture. Biochem. Soc. Trans. 44, 74–78 (2016).
Chong, S. L. et al. O-Acetylation of glucuronoxylan in Arabidopsis thaliana wild type and its change in xylan biosynthesis mutants. Glycobiology 24, 494–506 (2014).
Koutaniemi, S. et al. Substituent-specific antibody against glucuronoxylan reveals close association of glucuronic acid and acetyl substituents and distinct labeling patterns in tree species. Planta 236, 739–751 (2012).
Manabe, Y. et al. Reduced wall acetylation proteins play vital and distinct roles in cell wall O-acetylation in Arabidopsis. Plant Physiol. 163, 1107–1117 (2013).
Xiong, G., Cheng, K. & Pauly, M. Xylan O-acetylation impacts xylem development and enzymatic recalcitrance as indicated by the Arabidopsis mutant tbl29. Mol. Plant 6, 1373–1375 (2013).
Urbanowicz, B. R., Peña, M. J., Moniz, H. A., Moremen, K. W. & York, W. S. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 80, 197–206 (2014).
Bensussan, M. et al. Suppression of dwarf and irregular xylem phenotypes generates low-acetylated biomass lines in Arabidopsis. Plant Physiol. 168, 452–463 (2015).
Xiong, G., Dama, M. & Pauly, M. Glucuronic acid moieties on xylan are functionally equivalent to O-acetyl-substituents. Mol. Plant 8, 1119–1121 (2015).
Vršanská, M., Kolenová, K., Puchart, V. & Biely, P. Mode of action of glycoside hydrolase family 5 glucuronoxylan xylanohydrolase from Erwinia chrysanthemi. FEBS J. 274, 1666–1677 (2007).
Zhang, B. et al. Control of secondary cell wall patterning involves xylan deacetylation by a GDSL esterase. Nat. Plants 3, 17017 (2017).
Das, N. N., Das, S. C. & Mukherjee, A. K. On the ester linkage between lignin and 4-O-methyl-d-glucurono-d-xylan in jute fiber (Corchorus capsularis). Carbohydr. Res. 127, 345–348 (1984).
Lefebvre, V. et al. ESKIMO1 disruption in Arabidopsis alters vascular tissue and impairs water transport. PLoS ONE 6, e16645 (2011).
Kabel, M. A., van den Borne, H., Vincken, J. P., Voragen, A. G. J. & Schols, H. A. Structural differences of xylans affect their interaction with cellulose. Carbohydr. Polym. 69, 94–105 (2007).
Himmel, M. E. Biomass Recalcitrance: Deconstructing the Plant Cell Wall for Bioenergy (Blackwell Publishing Ltd, Oxford, 2009).
Xin, Z. & Browse, J. eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proc. Natl Acad. Sci. USA 95, 7799–7804 (1998).
Li, X. et al. Development and application of a high throughput carbohydrate profiling technique for analyzing plant cell wall polysaccharides and carbohydrate active enzymes. Biotechnol. Biofuels 6, 94 (2013).
Rogowski, A. et al. Glycan complexity dictates microbial resource allocation in the large intestine. Nat. Commun. 6, 7481 (2015).
Gonçalves, V. M. F., Evtuguin, D. V. & Domingues, M. R. M. Structural characterization of the acetylated heteroxylan from the natural hybrid Paulownia elongata/Paulownia fortunei. Carbohydr. Res. 343, 256–266 (2008).
Günl, M., Gille, S. & Pauly, M. OLIgo Mass Profiling (OLIMP) of extracellular polysaccharides. J. Vis. Exp. 40, e2046 (2010).
Enebro, J. & Karlsson, S. Improved matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry of carboxymethyl cellulose. Rapid Commun. Mass Spectrom. 20, 3693–3698 (2006).
Lesage, A., Bardet, M. & Emsley, L. Through-bond carbon-carbon connectivities in disordered solids by NMR. J. Am. Chem. Soc. 121, 10987–10993 (1999).
Fayon, F. et al. Through-space contributions to two-dimensional double-quantum J correlation NMR spectra of magic-angle-spinning solids. J. Chem. Phys. 122, 194313 (2005).
Fung, B. M., Khitrin, A. K. & Ermolaev, K. An improved broadband decoupling sequence for liquid crystals and solids. J. Magn. Reson. 142, 97–101 (2000).
Mortimer, J. C. et al. An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. Plant J. 83, 413–426 (2015).
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).
The authors declare no competing financial interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Biotechnology for Biofuels (2019)
Structural organization of the cell wall polymers in compression wood as revealed by FTIR microspectroscopy
New Phytologist (2019)
Critical Review of Plant Cell Wall Matrix Polysaccharide Glycosyltransferase Activities Verified by Heterologous Protein Expression
Frontiers in Plant Science (2019)
Current Opinion in Biotechnology (2019)