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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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.
The authors declare no competing financial interests.
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)
Electron tomography volume showing a typical type I plasmodesmata pore with no visible cytoplasmic sleeve. (AVI 29289 kb)
Electron tomography volume of the type II plasmodesmata shown in Supplementary Fig. 5a,b. (AVI 27965 kb)
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) doi:10.1038/nplants.2017.82
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