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Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR

Author

Listed:
  • Thomas J. Simmons

    (Department of Biochemistry and Leverhulme Centre for Natural Material Innovation)

  • Jenny C. Mortimer

    (Department of Biochemistry and Leverhulme Centre for Natural Material Innovation
    Present address: Joint Bioenergy Institute, Lawrence Berkeley National Lab, Berkeley, California 94720, USA)

  • Oigres D. Bernardinelli

    (Department of Biochemistry and Leverhulme Centre for Natural Material Innovation
    Instituto de Física de São Carlos, Universidade de São Paulo
    University of Warwick
    Present address: Instituto de Química, Universidade Estadual de Campinas, Caixa Postal 6154, CEP 13084-862, Campinas, Brazil)

  • Ann-Christin Pöppler

    (University of Warwick)

  • Steven P. Brown

    (University of Warwick)

  • Eduardo R. deAzevedo

    (Instituto de Física de São Carlos, Universidade de São Paulo)

  • Ray Dupree

    (University of Warwick)

  • Paul Dupree

    (Department of Biochemistry and Leverhulme Centre for Natural Material Innovation)

Abstract

Exploitation of plant lignocellulosic biomass is hampered by our ignorance of the molecular basis for its properties such as strength and digestibility. Xylan, the most prevalent non-cellulosic polysaccharide, binds to cellulose microfibrils. The nature of this interaction remains unclear, despite its importance. Here we show that the majority of xylan, which forms a threefold helical screw in solution, flattens into a twofold helical screw ribbon to bind intimately to cellulose microfibrils in the cell wall. 13C solid-state magic-angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy, supported by in silico predictions of chemical shifts, shows both two- and threefold screw xylan conformations are present in fresh Arabidopsis stems. The twofold screw xylan is spatially close to cellulose, and has similar rigidity to the cellulose microfibrils, but reverts to the threefold screw conformation in the cellulose-deficient irx3 mutant. The discovery that induced polysaccharide conformation underlies cell wall assembly provides new principles to understand biomass properties.

Suggested Citation

  • Thomas J. Simmons & Jenny C. Mortimer & Oigres D. Bernardinelli & Ann-Christin Pöppler & Steven P. Brown & Eduardo R. deAzevedo & Ray Dupree & Paul Dupree, 2016. "Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR," Nature Communications, Nature, vol. 7(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms13902
    DOI: 10.1038/ncomms13902
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    Cited by:

    1. Qaseem, Mirza Faisal & Shaheen, Humaira & Wu, Ai-Min, 2021. "Cell wall hemicellulose for sustainable industrial utilization," Renewable and Sustainable Energy Reviews, Elsevier, vol. 144(C).
    2. Zhiyou Zong & Scott Mazurkewich & Caroline S. Pereira & Haohao Fu & Wensheng Cai & Xueguang Shao & Munir S. Skaf & Johan Larsbrink & Leila Lo Leggio, 2022. "Mechanism and biomass association of glucuronoyl esterase: an α/β hydrolase with potential in biomass conversion," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    3. Xiaoyue Chen & Graham A. Hudson & Charlotte Mineo & Bashar Amer & Edward E. K. Baidoo & Samantha A. Crowe & Yuzhong Liu & Jay D. Keasling & Henrik V. Scheller, 2023. "Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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