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Wood cellulose microfibrils have a 24-chain core–shell nanostructure in seed plants

Nature Plants volume 9, pages 1154–1168 (2023)Cite this article

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Abstract

Wood cellulose microfibril (CMF) is the most abundant organic substance on Earth but its nanostructure remains poorly understood. There are controversies regarding the glucan chain number (N) of CMFs during initial synthesis and whether they become fused afterward. Here, we combined small-angle X-ray scattering, solid-state nuclear magnetic resonance and X-ray diffraction analyses to resolve CMF nanostructures in native wood. We developed small-angle X-ray scattering measurement methods for the cross-section aspect ratio and area of the crystalline-ordered CMF core, which has a higher scattering length density than the semidisordered shell zone. The 1:1 aspect ratio suggested that CMFs remain mostly segregated, not fused. The area measurement reflected the chain number in the core zone (Ncore). To measure the ratio of ordered cellulose over total cellulose (Roc) by solid-state nuclear magnetic resonance, we developed a method termed global iterative fitting of T1ρ-edited decay (GIFTED), in addition to the conventional proton spin relaxation editing method. Using the formula N = Ncore/Roc, most wood CMFs were found to contain 24 glucan chains, conserved between gymnosperm and angiosperm trees. The average CMF has a crystalline-ordered core of ~2.2 nm diameter and a semidisordered shell of ~0.5 nm thickness. In naturally and artificially aged wood, we observed only CMF aggregation (contact without crystalline continuity) but not fusion (forming a conjoined crystalline unit). This further argued against the existence of partially fused CMFs in new wood, overturning the recently proposed 18-chain fusion hypothesis. Our findings are important for advancing wood structural knowledge and more efficient use of wood resources in sustainable bio-economies.

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Fig. 1: Proposed CMF structural models.
Fig. 2: SAXS analyses of intact wood.
Fig. 3: Wood analyses by ssNMR.
Fig. 4: Extrapolation of cellulose NMR spectra by GIFTED experiments.
Fig. 5: XRD analyses of intact wood.
Fig. 6: SAXS analyses of aged wood.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding authors on reasonable request. Source data are provided with this paper.

Code availability

The computer source code for GIFTED global fitting analysis is given in the Supplementary Code.

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Acknowledgements

We thank I. Burgert and Y. Nishiyama for useful manuscript discussions. We thank K. W. Tong, S. Chiao, B.-T. Lee, D. Lu and Y.-H. Chu for providing wood samples. We thank National Synchrotron Radiation Research Center, Taiwan, for the provision of beamtime at TPS-BL13A, TLS-BL23A and TLS-BL01C2 endstations. We thank U.-S. Jeng for assistance with SAXS measurements. We thank the NTU-AMS Laboratory for radiocarbon dating and NTU Instrument Center for NMR measurements. This research received no external funding.

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Authors and Affiliations

  1. State Key Laboratory of Vaccines for Infectious Diseases, Xiang An Biomedicine Laboratory, State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Innovation Platform for Industry-Education Integration in Vaccine Research, School of Public Health, Xiamen University, Xiamen, People’s Republic of China

    Hwan-Ching Tai

  2. Department of Chemistry, National Taiwan University, Taipei, Republic of China

    Chih-Hui Chang, Jer-Horng Lin, Qian-Yan Lin, Eric Chung-Yueh Yuan, Shu-Li Li & Jerry Chun Chung Chan

  3. School of Cultural Industry and Tourism and Cultural Industry Research Center, Fujian Social Science Research Base, Xiamen University of Technology, Xiamen, People’s Republic of China

    Wenjie Cai

  4. Instrumentation Center, National Taiwan University, Taipei, Republic of China

    Shing-Jong Huang

  5. Department of Life Science and Institute of Plant Biology, National Taiwan University, Taipei, Republic of China

    Ying-Chung Jimmy Lin

  6. Department of Materials Science and Engineering, National Taiwan University, Taipei, Republic of China

    Cheng-Si Tsao

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Contributions

C.H.C. and J.H.L. were involved in methodology, investigation and formal analysis. W.C. undertook conceptualization, methodology and resources. S.J.H. contributed to investigation and formal analysis. Q.Y.L., E.C.Y.Y. and S.L.L. were involved in investigation, software and formal analysis. Y.C.J.L. contributed to conceptualization. J.C.C.C., C.S.T. and H.C.T. undertook conceptualization, methodology, formal analysis and writing.

Corresponding authors

Correspondence to Hwan-Ching Tai, Jerry Chun Chung Chan or Cheng-Si Tsao.

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Nature Plants thanks James Kubicki, Nayomi Plaza and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 SAXS fitting models.

(a) The SAXS intensities of dry maple samples (ambient humidity) and fully wetted samples, together with model-fitted intensities based on circular cylinders with 1.1 nm radius and finite lengths. (b) Previous wood SAXS studies modelled CMFs as infinitely long cylinders16,21,25,40,41,42,43,44, which was equivalent to the 2D scattering model of hard discs, and the fitted diameter (D) was misinterpreted as CMF width. (c) Porod analysis for maple SAXS profile showing a smooth interface in the high-q region. (d) The SAXS profiles calculated by Eq. (1) based on different radii, in comparison with those calculated by Eq. (2) based on the same radius but different lengths. (e) This study considers the 3D scattering model of CMFs with core-shell structures and finite lengths (L). Three models are considered: circular cylinders (CYL), rectangular parallelepipeds (PARA), and elliptical cylinders (ELL). The crystalline-ordered core is shown in red and semidisordered shell in white. The cross-sectional aspect ratio is defined as x:y or A:B.

Extended Data Fig. 2 SAXS analyses of Chinese fir and catalpa wood.

The SAXS patterns of Chinese fir is shown in (a), and the curve fitting results with CYL, ELL, and PARA models are shown in (c–e). Corresponding results for catalpa are shown in (b) and (f–h). Sample size: three trees per species and three locations per tree were measured, n = 9.

Extended Data Fig. 3 PSRE analyses of Chinese fir and catalpa wood.

13C{1H} cross-polarization spectrum of Chinese fir (a) and catalpa (b), separated into subspectrum A for cellulosic components and subspectrum B for non-cellulosic components using the PSRE method. The deconvolution of subspectrum A are shown for Chinese fir (c) and catalpa (d). Four trees per species were measured.

Extended Data Fig. 4 Pulse sequence of the GIFTED experiment.

The filled rectangle denotes a \(\pi /2\) pulse. The spin-locking duration (\({\tau }_{{\rm{SL}}}\)) was systematically varied in the range of 0.3 to 20 ms, whereas the CP contact time was fixed at 2 ms.

Extended Data Fig. 5 NMR spectral deconvolution.

Deconvolution of reference compounds of Avicel cellulose (a), extracted spruce hemicellulose (b), and extracted maple hemicellulose (c). For (b) and (c), only the peaks inside the dashed boxes were taken for the subsequent analyses of the spruce and maple GIFTED spectra.

Extended Data Fig. 6 Optimization of NMR parameters for GIFTED experiments.

(a) 13C{1H} CPMAS spectra of spruce acquired with the recycle delay (rd) of 3 and 10 s. (b) 13C{1H} CPMAS spectra of spruce acquired with contact times (\({\tau }_{{\rm{CP}}})\) equal to 1, 2, and 3 ms. (c) 13C{1H} CPMAS spectra of spruce with spinning frequency (\({\nu }_{{\rm{S}}}\)) at 10 and 15 kHz. The spectrum in red was scaled up by 1.5 times for comparison.

Extended Data Fig. 7 Optimization of spin-locking conditions.

(a) 13C{1H} CPMAS spectrum of 13C-labelled bacterial cellulose. The experimental spectrum (black) was deconvoluted, where the spectral components were shown in dashed lines, and their sum was shown in green. (b) \({T}_{1\rho }\) dispersion of 13C-labelled bacterial cellulose under spin-locking field B1,SL 30, 50, and 70 kHz. The colours of dashed lines were consistent with those in (a). (TC: total cellulose, CC: crystalline cellulose, SC: semidisordered cellulose).

Extended Data Fig. 8 GIFTED spin-locking spectra.

\({T}_{1\rho }\)-edited 13C{1H} CPMAS (GIFTED) spectra of spruce (a) and maple (b) at various spin-locking durations. Spectra on the right-hand side were scaled up to match the intensity at 89.0 ppm to compare relative intensity difference. Spectral components of cellulose are labelled in green, and non-cellulose labelled in orange. The peak positions of hemicellulose in the region of 50–105 ppm are indicated by orange arrows. Different intensity attenuations were observed, especially the non-cellulose spectral components. (TC: total cellulose, CC: crystalline cellulose, SC: semidisordered cellulose, H: hemicellulose, L: lignin).

Extended Data Fig. 9 XRD analyses of Chinese fir and catalpa wood.

XRD patterns of Chinese fir (a) and catalpa (b), with peak deconvolution analyses in (c) and (d), respectively. Four trees per species were measured.

Extended Data Fig. 10 SAXS analyses of artificially aged spruce and maple wood.

SAXS profile comparisons for untreated spruce and spruce treated with KOH, Ca(OH)2, and hot water are shown in (a). The mean and standard deviation are plotted for cross-section areas (b) and cross-section aspect ratios (c). Sample size: untreated n = 9 (three location form three trees) and treated n = 3 (three locations per tree). The p values are calculated using two-tailed Welch’s t-test against untreated controls. (d) The mean and standard deviation are plotted for crystallite widths along the directions of (110), (1–10), and (200) (untreated n = 5, treated n = 1).

Source data

Supplementary information

Supplementary Information

Supplementary Tables 1–5.

Reporting Summary

Supplementary Code

GIFTED fitting code.

Source data

Source Data Fig. 2

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Fig. 6

Statistical source data.

Source Data Extended Data Fig. 10

Statistical source data.

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Tai, HC., Chang, CH., Cai, W. et al. Wood cellulose microfibrils have a 24-chain core–shell nanostructure in seed plants. Nat. Plants 9, 1154–1168 (2023). https://doi.org/10.1038/s41477-023-01430-z

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