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Plant plasmodesmata bridges form through ER-driven incomplete cytokinesis

Ziqiang P. Li, Hortense Moreau, Jules D. Petit, Tatiana Souza-Moraes, Marija Smokvarska, Jessica Perez-Sancho, Melina Petrel, Fanny Decoeur, Lysiane Brocard, Clément Chambaud, Magali Grison, Andrea Paterlini, Lucie Hoornaert, Amit S. Joshi, Etienne Gontier, William A. Prinz, Yvon Jaillais, Antoine Taly, Felix Campelo, Marie-Cécile Caillaud, Emmanuelle M. Bayer

Posted on: 9 January 2024 , updated on: 10 January 2024

Preprint posted on 13 December 2023

and

Plasmodesmata act as unconventional membrane contact sites regulating inter-cellular molecular exchange in plants

Jessica Pérez-Sancho, Marija Smokvarska, Marie Glavier, Sujith Sritharan, Gwennogan Dubois, Victor Dietrich, Matthieu Pierre Platre, Ziqiang Patrick Li, Andrea Paterlini, Hortense Moreau, Laetitia Fouillen, Magali S. Grison, Pepe Cana-Quijada, Tatiana Sousa Moraes, Françoise Immel, Valerie Wattelet, Mathieu Ducros, Lysiane Brocard, Clément Chambaud, Matej Zabrady, Yongming Luo, Wolfgang Busch, Jens Tilsner, Yrjö Helariutta, Jenny Russinova, Antoine Taly, Yvon Jaillais, Emmanuelle M. Bayer

Posted on: , updated on: 10 January 2024

Preprint posted on 18 December 2023

How to make connections – the role of MCTP proteins and the ER in plasmodesmata formation and cell-to-cell communication

Selected by Gwendolyn K. Kirschner

Background

Cytoplasmic connections between plant cells were first described by the botanist Eduard Tangl in the late 19th century (Tangl, 1880), and named “plasmodesmata” by Strasburger a few years later (Strasburger, 1901). Today we know that plasmodesmata (PDs) are membrane-lined channels that allow molecule movement between two cells (Brunkard and Zambryski, 2017). In vascular plants, PDs are composed of an external membrane that is continuous with the plasma membrane (PM). Strands of compressed endoplasmic reticulum (ER) – called “desmotubule” – run through the PD channel and connect two neighbouring cells (Brunkard and Zambryski, 2017). PDs are formed through the incomplete separation of two daughter cells during cell division through the prevention of membrane abscission.

Membrane contact sites (MCS), such as sites of contact between the PM and the ER, serve as platforms for the transfer of ions and other molecules between organs (Wang et al., 2023). But even though PDs comply with the general definition of MCS, it is currently unknown if they function as MCS. Two recent preprints led by Emmanuelle Bayer (Li et al., 2023; Pérez-Sancho et al., 2023) address the outstanding questions: which role does the ER have for PD bridge formation? Which proteins are involved? And do PDs act as MCS? For both studies, the authors analysed PDs in the root meristem of Arabidopsis (Arabidopsis thaliana).

Key findings

Li et al. – MCTPs prevent abscission of the ER during cytokinesis and facilitate the formation of PD bridges

In the first preprint (Li et al., 2023), the authors used different imaging techniques such as scanning transmission electron microscopy tomography and airy scan microscopy to visualize PD formation during mitosis. They found that the ER was excluded from the mitotic spindles, and when vesicles assembled at the cell plate, the ER started to accumulate there and maintained a continuity between cells through the cell plate during cytokinesis. The fenestrae in the cell plate shrank gradually during cell plate formation and either closed or developed into plasmodesmata.

Using electron tomography, the authors visualised ER membranes and found that at the stage when the cell plate fused with the side walls (cross-wall stage), all fenestrae showed a continuous ER spanning the cells, while at an earlier stage (fenestrated-sheet stage), only around 66 % of fenestrae showed ER continuity. The authors therefore asked if the ER cell-cell continuity through fenestrae was a prerequisite for PD formation. A semi-quantitative physical and computational model of PD-fenestrae morphology and energetics predicted that expansion of the cell plate energetically favoured fenestrae shrinking, but that the presence of the ER increased the energy barrier against complete sealing and stabilized fenestrae at a specific diameter.

Candidate proteins that could be involved in this process are the multiple C2 domains and transmembrane proteins (MCTPs). MCTPs are PD proteins that anchor in the ER through their transmembrane region. They are proposed to dock to the PM through lipid binding domains (Brault et al., 2019). By correlative light and electron microscopy and airy scan microscopy, the authors found that MCTP3, MCTP4, and MCTP6 localised uniformly to the ER-associated cell plate in dividing cells. Before the cross-wall transition, they accumulated at nascent PDs. A combination of fluorescence recovery after photobleaching (FRAP) and fluorescence loss in photobleaching (FLIP) experiments showed that the MCTPs were mobile before their accumulation at the PDs, but that from the cross-wall stage on their mobility decreased. The semi-quantitative physical model of PD formation confirmed that enrichment of MCTPs in contracting fenestrae was energetically favourable. Transmission electron microscopy and serial block-face scanning electron microscopy (SBF-SEM) showed that in mctp double (mctp3/mctp4) and triple mutants (mctp3/mctp4/mctp6), the number of PDs was reduced in comparison to wild type (WT) and that the PD number reduction originated at cytokinesis stage. In summary, this suggests that the MCTPs prevent abscission of the ER during cytokinesis and thereby facilitate the formation of stable intercellular bridges (Figure 1A-C).

Pérez-Sancho et al. – PD bridges function as unconventional MCS

But is ER-PM apposition relevant for PD function? And what is the role of the MCTPs? In the second preprint, the authors looked at the MCTPs as core constituents of PDs (Pérez-Sancho et al., 2023). mctp double mutants (mctp3/mctp4, mctp4/mctp6) were affected in shoot and root development, while mctp3/mctp4/mctp6 triple mutants were not viable on soil. Co-immunoprecipitation experiments in Nicotiana benthamiana as well as Förster Resonance Energy Transfer Fluorescence Lifetime Imaging Microscopy (FRET-FLIM) analysis in Arabidopsis showed that MCTP3, MCTP4 and MCTP6 were able to form hetero-oligomers. This suggests that MCTP3, MCTP4 and MCTP6 interact on both a physical and genetic level.

By using electron tomography, the authors then showed that WT PDs exhibited very tight ER-PM contacts, while in the mctp triple mutant, a majority of PDs showed ER and PM membrane detachment.  Using the cytosolic dye carboxyfluorescein diacetate (CFDA) and FRAP, as well as the reversibly switchable photoactivatable fluorescent marker DRONPA, the authors showed that molecule movement between cells increased in the mctp double mutants, indicating that altered ER-PM contact at the PDs modified PD transport activity in the double mutants. PD cell-cell trafficking is regulated by callose, among others, which reduces cell-cell transport by accumulating at the PDs (Amsbury et al., 2017). Therefore, the authors tested callose deposition and molecule movement after hormone and stress treatments known to affect PDs and found that ER-PM tethering has a dominant role over callose function to regulate PD closure.

MCTPs dock to the PM by interacting with anionic lipids through their C2-lipid binding domain (Brault et al., 2019). The authors confirmed the presence of the phosphoinositide PI4P, a prime determinant of the PM inner leaflet electrostatic signature in plants (Simon et al., 2016) at the PDs. To analyse the impact of PI4P on cell-cell trafficking, they used PI4P inhibitors and found that these increased cell-cell trafficking in WT but not in the mctp double mutants. Vice versa, mutants with increased PI4P levels showed reduced cell-cell trafficking. The authors created near-atomistic structural and energetic models to analyse the interaction of MCTP4 with the PM and found that PI4P increased the frequency of binding between the C2 domains and the PM, suggesting a role in stabilizing docking of MCTPs to the PM. Altogether, this suggests that PD bridges function as unconventional MCS, and that the regulation of the membrane contacts involves protein tethers and phosphoinositides to control cell-cell trafficking (Figure 1D).

What I like about the preprints

I chose these two preprints because the authors use different state-of-the art high resolution imaging techniques that align well with the respective scientific questions. The outcome of the studies enhances our understanding of the mechanism of PD formation as well as their role in cell-cell communication.

Figure 1: Plasmodesmata (PDs) are formed by incomplete abscission of the ER. ER and plasma membrane (PM) function as membrane contact sites (MCS) in the PDs to regulate cell-cell trafficking.
During the fenestrated-sheet stage, multiple C2 domains and transmembrane proteins (MCTPs, magenta) are localised to the ER (green) associated with the cell plate (gray) (A); in the cross-wall stage, MCTPs accumulate at the PDs (B); MCTPs prevent abscission of the ER during cytokinesis; after cytokinesis, the fenestrae have formed stable intercellular bridges (C).
The PD MCS are regulated by MCTPs that act as tethers between PM (blue) and ER membranes, with PM-localized PI4P lipid (yellow) as a binding partner (D).

 

References

Amsbury, S., Kirk, P. and Benitez-Alfonso, Y. (2017) Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J. Exp. Bot., 69, 105–115.

Brault, M.L., Petit, J.D., Immel, F., et al. (2019) Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep., 20, 1–26.

Brunkard, J.O. and Zambryski, P.C. (2017) Plasmodesmata enable multicellularity: new insights into their evolution, biogenesis, and functions in development and immunity. Curr. Opin. Plant Biol., 35, 76–83.

Li, Z.P., Moreau, H., Petit, J.D., et al. (2023) Plant plasmodesmata bridges form through ER-driven incomplete cytokinesis. bioRxiv.

Pérez-Sancho, J., Smokvarska, M., Glavier, M., et al. (2023) Plasmodesmata act as unconventional membrane contact sites regulating inter-cellular molecular exchange in plants. bioRxiv.

Simon, M.L.A., Platre, M.P., Marquès-Bueno, M.M., Armengot, L., Stanislas, T., Bayle, V., Caillaud, M.C. and Jaillais, Y. (2016) A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat. Plants, 2, 1–10.

Strasburger, E. (1901) Über plasmaverbindungen pflanzlicher zellen, Gebr. Borntraeger.

Tangl, E. (1880) Ueber offene Communicationen zwischen den Zellen des Endosperms einiger Samen. Jb wiss Bot, 12, 170–190.

Wang, P., Duckney, P., Gao, E., Hussey, P.J., Kriechbaumer, V., Li, C., Zang, J. and Zhang, T. (2023) Keep in contact: multiple roles of endoplasmic reticulum–membrane contact sites and the organelle interaction network in plants. New Phytol., 238, 482–499.

 

 

doi: https://doi.org/10.1242/prelights.36324

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