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Nanoscale movements of cellulose microfibrils in primary cell walls

Nature Plants volume 3, Article number: 17056 (2017) Cite this article

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An Author Correction to this article was published on 26 November 2020

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Abstract

The growing plant cell wall is commonly considered to be a fibre-reinforced structure whose strength, extensibility and anisotropy depend on the orientation of crystalline cellulose microfibrils, their bonding to the polysaccharide matrix and matrix viscoelasticity1–4. Structural reinforcement of the wall by stiff cellulose microfibrils is central to contemporary models of plant growth, mechanics and meristem dynamics4–12. Although passive microfibril reorientation during wall extension has been inferred from theory and from bulk measurements13–15, nanometre-scale movements of individual microfibrils have not been directly observed. Here we combined nanometre-scale imaging of wet cell walls by atomic force microscopy (AFM) with a stretching device and endoglucanase treatment that induces wall stress relaxation and creep, mimicking wall behaviours during cell growth. Microfibril movements during forced mechanical extensions differ from those during creep of the enzymatically loosened wall. In addition to passive angular reorientation, we observed a diverse repertoire of microfibril movements that reveal the spatial scale of molecular connections between microfibrils. Our results show that wall loosening alters microfibril connectivity, enabling microfibril dynamics not seen during mechanical stretch. These insights into microfibril movements and connectivities need to be incorporated into refined models of plant cell wall structure, growth and morphogenesis.

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Figure 1: Microfibril reorientations during different modes of cell wall extension.
Figure 2: Diversity of individual microfibril movements during cell wall extension.
Figure 3: Modulus maps of cell wall surface after different modes of extension.

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Change history

  • 26 November 2020

    A Correction to this paper has been published: https://doi.org/10.1038/nplants.2017.56.

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Acknowledgements

This work was supported as part of the Center for LignoCellulose Structure and Formation, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, Basic Energy Sciences under award no. DE-SC0001090. D.V. was supported by NIH grant R01GM098430. We thank E. Wagner, X. Wang, S. Kiemle and Y. B. Park for technical assistance.

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Authors and Affiliations

  1. Department of Biology and Center for Lignocellulose Structure and Formation, Penn State University, University Park, 208 Mueller Laboratory, 16802, Pennsylvania, USA

    Tian Zhang, Daniel M. Durachko & Daniel J. Cosgrove

  2. Department of Physics, Lehigh University, Bethlehem, 18015, Pennsylvania, USA

    Dimitrios Vavylonis

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  1. Tian Zhang
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  3. Daniel M. Durachko
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  4. Daniel J. Cosgrove
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Contributions

T.Z. carried out the AFM experiments and analysed the data. D.V. assisted with SOAX analysis of microfibril orientations. D.M.D. designed and built the AFM extensometer. D.J.C. designed the research and analysed the data. T.Z., D.J.C. and D.V. wrote the manuscript.

Corresponding author

Correspondence to Daniel J. Cosgrove.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1-5, Legends for Supplementary Videos 1-4. (PDF 683 kb)

Supplementary Video 1

Animated GIF showing negligible microfibril movement during Cel12A-induced stress relaxation. (GIF 428 kb)

Supplementary Video 2

Animated GIF to compare microfibril positions before and after plastic extension. (GIF 716 kb)

Supplementary Video 3

Animated GIF showing microfibril movement during elastic extension. (GIF 686 kb)

Supplementary Video 4

Animated GIF showing microfibril movement during Cel12A-induced creep. (GIF 695 kb)

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Zhang, T., Vavylonis, D., Durachko, D. et al. Nanoscale movements of cellulose microfibrils in primary cell walls. Nature Plants 3, 17056 (2017). https://doi.org/10.1038/nplants.2017.56

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