Letter

Nanoscale movements of cellulose microfibrils in primary cell walls

  • Nature Plants 3, Article number: 17056 (2017)
  • doi:10.1038/nplants.2017.56
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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,​2,​3,​4. Structural reinforcement of the wall by stiff cellulose microfibrils is central to contemporary models of plant growth, mechanics and meristem dynamics4,​5,​6,​7,​8,​9,​10,​11,​12. Although passive microfibril reorientation during wall extension has been inferred from theory and from bulk measurements13,​14,​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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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.

Author information

Affiliations

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

    • Tian Zhang
    • , Daniel M. Durachko
    •  & Daniel J. Cosgrove
  2. Department of Physics, Lehigh University, Bethlehem, Pennsylvania 18015, USA

    • Dimitrios Vavylonis

Authors

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Daniel J. Cosgrove.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1-5, Legends for Supplementary Videos 1-4.

Image files

  1. 1.

    Supplementary Video 1

    Animated GIF showing negligible microfibril movement during Cel12A-induced stress relaxation.

  2. 2.

    Supplementary Video 2

    Animated GIF to compare microfibril positions before and after plastic extension.

  3. 3.

    Supplementary Video 3

    Animated GIF showing microfibril movement during elastic extension.

  4. 4.

    Supplementary Video 4

    Animated GIF showing microfibril movement during Cel12A-induced creep.