Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR
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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. 13 C 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.
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Such structural rearrangements have been observed in the xylan of the secondary cell walls across various plant species, where folding onto the flat surfaces of cellulose microfibrils induces a conformational shift from a three-fold helical structure to a flat, two-fold conformation.
“Such structural rearrangements have been observed in the xylan of the secondary cell walls across various plant species, where folding onto the flat surfaces of cellulose microfibrils induces a conformational shift from a three-fold helical structure to a flat, two-fold conformation92–94.”
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BackgroundInfluentialDickwella Widanage, M. C., Gautam, I., Sarkar, D., Mentink-Vigier, F., Vermaas, J. V., Ding, S.-Y., Lipton, A. S., Fontaine, T., Latgé, J.-P., Wang, P., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-50799-8 · Cited by 70 · see citing works
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“Xylan has recently been shown to interact with the hydrophilic surface and perhaps also the hydrophobic surface of cellulose microfibrils as a 2-fold helical screw (Busse-Wicher et al., 2014; Simmons et al., 2016; Grantham et al., 2017).”
BackgroundSelf-citationMolecular understanding of wood formation in trees
Luo, L., & Li, L.-G. (2022) · Forestry Research · doi:10.48130/fr-2022-0005 · Cited by 67 · see citing works
Poulhazan, A., Widanage, M. C. D., Muszyński, A., Arnold, A., Warschawski, D., Azadi, P., Marcotte, I., & Wang, T. (2021) · Journal of the American Chemical Society · doi:10.1021/jacs.1c07429 · Cited by 66 · see citing works
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“The even GlcA spacing facilitates binding to cellulose microfibrils through a twofold helical screw ribbon conformation of the glucuronoxylan, which probably exerts an influence on microfibril aggregation and organization (Simmons et al., 2016).”
BackgroundSelf-citationCCMRD: a solid-state NMR database for complex carbohydrates
Kang, X., Zhao, W.-C., Widanage, M. C. D., Kirui, A., Ozdenvar, U., & Wang, T. (2020) · Journal of Biomolecular NMR · doi:10.1007/s10858-020-00304-2 · Cited by 64 · see citing works
Two Complementary Mechanisms Underpin Cell Wall Patterning during Xylem Vessel Development[OPEN]
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Atomistic, macromolecular model of the Populus secondary cell wall informed by solid-state NMR
Addison, B., Bu, L., Bharadwaj, V. S., Crowley, M. F., Harman-Ware, A. E., Crowley, M. F., Bomble, Y., & Ciesielski, P. N. (2024) · Science Advances · doi:10.1126/sciadv.adi7965 · Cited by 63
“The 2 1 conformation of β (1–4) linked glycans is characterized by a φ + ψ sum ~ 120°, whereas the 3 1 conformation is characterized by a φ + ψ sum ~ 50° or 190° ( 17 , 25 , 42 , 43 ).”
InfluentialYang, X., Jungstedt, E., Reid, M. S., & Berglund, L. (2021) · doi:10.1021/acs.macromol.1c00305 · Cited by 63
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Fliri, L., Heise, K., Koso, T. V., Todorov, A. R., del Cerro, D. R., Hietala, S., Fiskari, J., Kilpeläinen, I., Hummel, M., & King, A. W. T. (2023) · Nature Protocols · doi:10.1038/s41596-023-00832-9 · Cited by 78 · see citing works
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“The major domain xylan, rather than clumping with each other, enters into grooves present on the hydrophilic face of microfibrils, attaches them through hydrogen bonding, and forms a layer on the outer face of cellulose [79,81].”
BackgroundLyczakowski, J. J., Bourdon, M., Terrett, O. M., Helariutta, Y., Wightman, R., & Dupree, P. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01398 · Cited by 60 · see citing works
Self-citationTemple, H., Phyo, P., Yang, W.-B., Lyczakowski, J. J., Echevarría-Poza, A., Yakunin, I., Parra-Rojas, J., Terrett, O. M., Saez-Aguayo, S., Dupree, R., et al. (2022) · Nature Plants · doi:10.1038/s41477-022-01156-4 · Cited by 58
“WT and gosamt1 gosamt2 plants were grown in a custom-designed growth chamber and were enriched in 13 C using CO 2 as previously described 53 .”
InfluentialSelf-citationRodrigues, R. C. L. B., Rodrigues, B. G., Canettieri, E. V., Martinez, E. A., Palladino, F., Wisniewski, A., & Rodrigues, D. (2021) · Bioresource Technology · doi:10.1016/j.biortech.2021.126627 · Cited by 58 · see citing works
Importance of Water in Maintaining Softwood Secondary Cell Wall Nanostructure
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Self-citationThermal reactivity of hemicellulose and cellulose in cedar and beech wood cell walls
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Interactions between callose and cellulose revealed through the analysis of biopolymer mixtures
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Renewable hemicellulose-based materials for value-added applications
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How Many Glucan Chains Form Plant Cellulose Microfibrils? A Mini Review
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Self-citationDegumming of Hemp Fibers Using Combined Microwave Energy and Deep Eutectic Solvent Treatment
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“According to the literature, the chemical shift at 64 ppm could be assigned to the carbon-5 of xylan or hemicellulose (Simmons et al., 2016), and this signal was flattened after DES and alkali treatment, indicating the removal of”
BackgroundGrass secondary cell walls, Brachypodium distachyon as a model for discovery.
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“The nature and patterning of these side chains have major impacts on cell wall integrity, mediating xylan–cellulose and xylan–lignin polymer interactions (Simmons et al., 2016; Mart ınez-Abad et al., 2017).”
BackgroundArabinose substitution effect on xylan rigidity and self-aggregation
Shrestha, U. R., Smith, S., Pingali, S., Yang, H., Zahran, M., Breunig, L., Wilson, L. A., Kowali, M., Kubicki, J., Cosgrove, D., et al. (2019) · Cellulose · doi:10.1007/s10570-018-2202-8 · Cited by 55
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Eudicot primary cell wall glucomannan is related in synthesis, structure, and function to xyloglucan
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“Indeed, the regular pattern of substitution of xylan, an unrelated hemicellulose, is thought to influence the binding of xylan to cellulose in secondary cell walls (SCWs) (Simmons et al., 2016; Grantham et al., 2017).”
BackgroundInfluentialSelf-citationThe Dynamic Responses of Cell Walls in Resurrection Plants During Dehydration and Rehydration
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“In other words, hemicellulose, instead of lignin, might be the main cellular component responsible for resisting the widening of the spacing between microfibrils, which is considered a key factor for controlling the growth rate of plant cell walls [47].”
BackgroundRecent advance on lignin-containing nanocelluloses: The key role of lignin.
Hu, M.-T., Lv, X., Wang, Y., Ma, L., Zhang, Y.-H., & Dai, H. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122460 · Cited by 53
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Arabinosyl Deacetylase Modulates the Arabinoxylan Acetylation Profile and Secondary Wall Formation
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“Disrupting the characteristic acetylation profile on the Arabidopsis (Arabidopsis thaliana) xylan backbone causes xylan misfolding and interferes with the interactions with cellulose 1Address correspondence to: bczhang@genetics.ac.cn and yhzhou@ genetics.ac.cn.”
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Water as an Intrinsic Structural Element in Cellulose Fibril Aggregates
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“A general look at these results [94,95] shows that lignin is strongly associated with xylan and GGM bound to cellulose, and some lignin is close to the cellulose surface (cellulose domain 2) [63].”
BackgroundHydrochar Production by Hydrothermal Carbonization: Microwave versus Supercritical Water Treatment
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“…of carbon, making it a promising material for various applications, including soil amendment, energy generation, and environmental remediation [49]. energy During hydrothermal carbonization, biomass undergoes complex chemical reactions involving dehydration, decarboxylation, and…”
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- Authors
- Simmons, T. J., Mortimer, J. C., Bernardinelli, O. D., Pöppler, A.-C., Brown, S. P., deAzevedo, E. R., Dupree, R., & Dupree, P.
- Affiliations
- University of Cambridge (GB)
- Universidade de São Paulo (BR)
- University of Warwick (GB)
- Corresponding author
- Dupree, Ray
- Dupree, Paul
- ORCID
- Venue
- Nature Communications
- Published
- 2016-12-21
- Volume
- 7
- Issue
- 1
- Pages
- 13902-13902
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC5187587
- OpenAlex
- W2562144926
- Cited by
- 436
- References
- 51
- Citations by year
- 2026: 47 · 2025: 50 · 2024: 45 · 2023: 35 · 2022: 54 · 2021: 51 · 2020: 56 · 2019: 39 · 2018: 40 · 2017: 19
- FWCI
- 38.04
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Americanae (AECID Library) (publishedVersion, other-oa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Warwick Research Archive Portal (University of Warwick) (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- Advantage West Midlands
- Leverhulme Trust
- Royal Society
- University of Warwick
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (2011-6, 2014-4)
- Engineering and Physical Sciences Research Council (PR140003, EP/F017901/1, UK 850 MHz solid-state NMR Facility)
- Biotechnology and Biological Sciences Research Council (BB/G016240/1, PR140003)
- European Regional Development Fund
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
- Life Sciences › Agricultural and Biological Sciences › Food Science › Polysaccharides Composition and Applications
- Physical Sciences › Materials Science › Biomaterials › Advanced Cellulose Research Studies
- Keywords
- xylan, cellulose microfibrils, plant cell wall, polysaccharide conformation, lignocellulosic biomass, cell wall assembly, non-cellulosic polysaccharides
- MeSH terms
- Carbohydrate Conformation, Carbohydrate Sequence, Carbon Isotopes, Cell Wall, Cellulose, Mutation, Magnetic Resonance Spectroscopy, Xylans, Arabidopsis, Plant Stems, Plant Cells
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