Specialized membrane domains of plasmodesmata, plant intercellular nanopores

  • Bayer E
  • Mongrand S
  • Tilsner J
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Abstract

Keywords: plasmodesmata, lipid rafts, membrane microdomains, membrane curvature, plasma membrane, endoplasmic reticulum, super-resolution microscopy, protein-lipid interaction Plasmodesmata (PD) are plant-specific membrane-lined chan-nels that connect neighboring cells across the cell wall and are indispensable for intercellular communication, development and defense against pathogens. They consist of concentric membrane tubules of the plasma membrane (PM) on the outside and endo-plasmic reticulum (ER) on the inside. The biophysical properties and molecular composition of both membranes are most likely distinct from the respective bulk membranes with which they are continuous. This specialization of PD membranes is expected to guarantee not only the compartmentalization of PD-related func-tion but also to accommodate the requirement for highly curved membrane organization (Mongrand et al., 2010; Tilsner et al., 2011). This Research Topic brings together researchers from a variety of areas to apply the significant recent advances in understanding how the interactions of lipids and proteins influence the behav-ior and spatial/functional compartmentalization of biological membranes on PD-related questions. The first several contributions are focussed on the molecular and physical properties of the PD plasma membrane (PD-PM). The PD-PM contains a different set of proteins than the PM out-side the channels and does not permit free diffusion of membrane components between cells, indicating that it is laterally segre-gated from the bulk PM and forms a membrane microdomain (or several). In line with a view of microdomains as signaling " hubs, " PD have recently been emerging as important sites of pathogen-related and developmental signaling. Faulkner (2013) reviews the currently identified PD-located receptors and sug-gests that sub-division of the PD-PM into microdomains, be it raft-like or tetraspanin webs, may facilitate signaling pro-cesses through the local clustering of membrane components. Preferential compartmentation of proteins but also lipids into membrane microdomains have been postulated for many cell types, but have long been difficult to directly visualize in vivo. Owen and Gaus (2013) and Truong-Quang and Lenne (2014) both review how recent advantages in light microscopy that allow imaging below the diffraction limit can be used to obtain new insights into the dynamics of microdomains and to draw con-clusions on the mechanism of their formation. Truong-Quang and Lenne review internal structuring as well as higher-order clustering of microdomains. Owen and Gaus discuss their recent findings from direct imaging of PM lipid order in vivo. They found the PM to consist of ∼75% liquid-ordered (L o) and 25% liquid-disordered (L d) sub-resolution microdomains and postu-late that small changes in lipid phase distribution can induce rapid large-scale changes in protein geometry of the PM when a lipid phase switches from being the " island " to the " percolating " phase and vice versa. So far no data exist as to how lateral membrane heterogeneity and compartmentalization of biological processes are achieved at PD. In other words, how are locally confined PD membrane sites established and maintained within the pore, despite their conti-nuity with the bulk membranes outside PD? What mechanisms restrict lateral mobility of proteins and possibly lipids along the PD membranes? A number of articles ask how a laterally segregated PM domain could be maintained at PD (and elsewhere). One potential mech-anism for microdomain formation is the " picket fence " model which suggests that, in mammalian cells at least, PM domains are corralled by structural elements attached to the membrane and underlying cytoskeleton. In plant cells different mechanisms might be at work. Martinière and Runions (2013) review their recent experimental findings showing that compared to animal cells, most of the plant PM-resident proteins display a low mobil-ity and that restricted lateral diffusion depends mostly on the cell wall. Intricate connections between the PD-PM and surround-ing wall have been observed and are likely to contribute to the specialization of this membrane domain. Boutté and Moreau (2014) review the role of small GTPases in PM partitioning and suggest that such mechanisms could also act at PD. Several small GTPases have been found in the PD proteome and could potentially be involved in specifying the PD-PM. In line with the idea that the PD-PM may cluster L o sterol and sphingolipid enriched raft microdomains, a number of articles provide insights about the potential contribution of lipid phase separation to the selective lateral segregation of PD components. de Almeida and Joly (2014) suggest that nano-scale lipid phase separation may also include the formation of solid-ordered/gel (S o) phases around nucleating oligomers of membrane-integral proteins or lipids, which could stabilize membrane microdomains for longer time spans than the L o domains of the conventional raft hypothesis. Whilst still speculative at this stage, such a model could potentially provide an explanation for the restricted lat-eral diffusion within the PD-PM. On their side Bagatolli and www.frontiersin.org September 2014 | Volume 5 | Article 507 | 1

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Bayer, E. M., Mongrand, S., & Tilsner, J. (2014). Specialized membrane domains of plasmodesmata, plant intercellular nanopores. Frontiers in Plant Science, 5. https://doi.org/10.3389/fpls.2014.00507

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