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Architecture and permeability of post-cytokinesis plasmodesmata lacking cytoplasmic sleeves

Nature Plants volume 3, Article number: 17082 (2017) Cite this article

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Abstract

Plasmodesmata are remarkable cellular machines responsible for the controlled exchange of proteins, small RNAs and signalling molecules between cells. They are lined by the plasma membrane (PM), contain a strand of tubular endoplasmic reticulum (ER), and the space between these two membranes is thought to control plasmodesmata permeability. Here, we have reconstructed plasmodesmata three-dimensional (3D) ultrastructure with an unprecedented level of 3D information using electron tomography. We show that within plasmodesmata, ER–PM contact sites undergo substantial remodelling events during cell differentiation. Instead of being open pores, post-cytokinesis plasmodesmata present such intimate ER–PM contact along the entire length of the pores that no intermembrane gap is visible. Later on, during cell expansion, the plasmodesmata pore widens and the two membranes separate, leaving a cytosolic sleeve spanned by tethers whose presence correlates with the appearance of the intermembrane gap. Surprisingly, the post-cytokinesis plasmodesmata allow diffusion of macromolecules despite the apparent lack of an open cytoplasmic sleeve, forcing the reassessment of the mechanisms that control plant cell–cell communication.

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Figure 1: Plasmodesmata ER–PM contact site morphology evolves during tissue development in root tips.
Figure 2: The spoke-like tethering elements of type II plasmodesmata correlate with ER–PM spacing and are not sensitive to F-actin polymerization inhibitor drugs.
Figure 3: Very tight ER–PM contact in post-cytokinesis plasmodesmata.
Figure 4: Very tight ER–PM contacts are established during cell plate formation.
Figure 5: Molecular trafficking through type I plasmodesmata.

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Acknowledgements

This work was supported by the grants by the Region Aquitaine (to E.M.B) and PEPS (Initial Support for Exploratory Projects to E.M.B) and National Agency for Research (Grant ANR-14-CE19-0006-01 to E.M.B). Electron and fluorescence microscopy analyses were performed at the Bordeaux Imaging Centre (http://www.bic.u-bordeaux.fr/). The Region Aquitaine also supported the acquisition of the electron microscope (grant no. 2011 13 04 007 PFM). We thank Y. Benitez-Alfonso for providing the Arabidopsis PA–GFP lines and S. Mongrand, V. Arondel, Y. Boutté, Y. Jaillais and C. Hawes for critical review of the article before submission.

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  1. Amélia Gaston & Mathieu Fouché

    Present address: UMR 1332 BFP, INRA, University of Bordeaux, 33140, Villenave d'Ornon Cedex, France

Authors and Affiliations

  1. Laboratory of Membrane Biogenesis, UMR5200 CNRS, University of Bordeaux, 71 Avenue Edouard Bourlaux, 33883 Villenave d'Ornon Cedex, France

    William J. Nicolas, Magali S. Grison, Amélia Gaston, Mathieu Fouché & Emmanuelle M. Bayer

  2. Institut Curie, Centre de Recherche, Bât. 112, Centre Universitaire, 91405 Orsay Cedex, France

    Sylvain Trépout

  3. Bordeaux Imaging Centre, UMS 3420 CNRS, CNRS-INSERM-University of Bordeaux 146, rue Léo Saignat, 33076 Bordeaux Cedex, France

    Fabrice P. Cordelières

  4. Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh, EH9 3BF, UK

    Karl Oparka

  5. Biomedical Sciences Research Complex, University of St Andrews, KY16 9ST, St Andrews, UK

    Jens Tilsner

  6. Cell and Molecular Sciences, James Hutton Institute, DD2 5DA, Dundee, UK

    Jens Tilsner

  7. Bordeaux Imaging Centre, Plant Imaging Plateform, UMS 3420, INRA-CNRS-INSERM-University of Bordeaux, 71 Avenue Edouard Bourlaux, 33883 Villenave-d'Ornon Cedex, France

    Lysiane Brocard

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Contributions

Electron microscopy and associated-quantitative analyses were done by W.J.N. with the help of S.T. and L.B. M.S.G. performed the cell-to-cell connectivity essays with the help of W.J.N and L.B. F.P.C. and L.B. provided technical support for the FRAP experiments and with image quantification and acquisition. All statistical analyses were run by W.J.N. and M.S.G. A.G. and M.F. performed the control tests for latrunculin and cytochalasin treatments in the roots. The manuscript was written by E.M.B. and W.J.N. with contributions of L.B., K.O. and J.T. Research was designed by E.M.B.

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Correspondence to Lysiane Brocard or Emmanuelle M. Bayer.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figure 1, Supplementary Figure 3, Supplementary Figure 5, Supplementary Figure 8. (PDF 5630 kb)

Supplementary Video 2: Cytoplasmic streaming of Golgi vesicles is altered upon inhibition of actin polymerization

Timelapse of Mb12:YFP lines (a–c) and Ng1:GFP lines (d–f) taken at t = 0, 30 min and 1 h of treatment at 1 image every 5 seconds. (AVI 3575 kb)

Supplementary Video 4: Type I plasmodesmata in Arabidopsis cultured cells

Electron tomography volume showing a typical type I plasmodesmata pore with no visible cytoplasmic sleeve. (AVI 29289 kb)

Supplementary Video 6: Type II plasmodesmata in Arabidopsis cultured cells

Electron tomography volume of the type II plasmodesmata shown in Supplementary Fig. 5a,b. (AVI 27965 kb)

Supplementary Video 7: Type II plasmodesmata in Arabidopsis cultured cells

Electron tomography volume of the type II plasmodesmata exhibited in Supplementary Fig. 5c,d. (AVI 17357 kb)

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Nicolas, W., Grison, M., Trépout, S. et al. Architecture and permeability of post-cytokinesis plasmodesmata lacking cytoplasmic sleeves. Nature Plants 3, 17082 (2017). https://doi.org/10.1038/nplants.2017.82

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