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

Nature Plants volume 3, pages 859–865 (2017)Cite this article

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Abstract

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.

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Fig. 1: U(Me) decoration patterns are disrupted in esk1 but not rwa acetylation mutants.
Fig. 2: Both GUX1 and GUX2 contribute to glucuronosylation in the esk1 mutant, but GUX1 is deregulated in its patterning activity.
Fig. 3: Solid-state NMR of WT and esk1kak mutant cell walls shows that the unpatterned xylan does not bind to cellulose in the twofold screw conformation found in WT plants.
Fig. 4: A model of glucuronoxylan substitution pattern generation and its consequence for xylan interaction with cellulose.

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Acknowledgements

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).

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Authors and Affiliations

  1. Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QW, UK

    Nicholas J. Grantham, Joel Wurman-Rodrich, Oliver M. Terrett, Jan J. Lyczakowski, Katherine Stott, Thomas J. Simmons, Marta Busse-Wicher & Paul Dupree

  2. Department of Physics, University of Warwick, Coventry, CV4 7AL, UK

    Dinu Iuga, Steven. P. Brown & Ray Dupree

  3. Institut Jean-Pierre Bourgin, UMR 1318, INRA AgroParisTech CNRS, Université Paris-Saclay, 78026, Versailles Cedex, France

    Mylene Durand-Tardif

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Contributions

N.J.G. conducted most of the plant molecular genetic and biochemical experiments, assisted by J.W.-R. and M.B.-W. M.D.-T. provided esk1kak genetic material and supporting information. The solid-state NMR experiments were conducted by R.D. assisted by D.I. using plants grown by T.J.S., O.M.T. and J.J.L. Solution NMR was conducted by K.S. and N.J.G. Data analysis was conducted by N.J.G., J.W.-R., O.M.T., J.J.L., K.S., T.J.S., M.B.-W., S.P.B., R.D. and P.D. M.B.-W., S.P.B., R.D. and P.D. supervised aspects of the project. The paper was written by N.J.G., M.B.-W. and P.D. with contributions from all authors.

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Correspondence to Paul Dupree.

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Grantham, N.J., Wurman-Rodrich, J., Terrett, O.M. et al. An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls. Nature Plants 3, 859–865 (2017). https://doi.org/10.1038/s41477-017-0030-8

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