Plasmodesmata and the control of symplastic transport

Abstract

'There are holes in the sky where the rain gets in, but they're ever so small that's why rain's so thin' In 1879 Eduard Tangle discovered cytoplasmic connections between cells in the cotyledons of Strychnos nuxvomica, which he interpreted to be protoplasmic contacts. This led him to hypothesize that 'the protoplasmic bodies . . . are united by thin strands passing through connecting ducts in the walls, which put the cells into connection with each other and so unite them to an entity of higher order' (Carr 1976). This challenged the then current view that cells functioned as autonomous units. It was after much research in many other species and cell types that Strasburger, in 1901, named these structures plasmodesmata (Carr 1976). During the division and differentiation of meristematic cells, plasmodesmata are formed across each developing cell plate, allowing cytoplasmic and endomembrane continuity to occur between all daughter cells, and ultimately, between all cells in a developing tissue (Mezitt & Lucas 1996). Those plasmodesmata that form during cell division are termed primary plasmodesmata (Jones 1976). Those that form de novo across existing cell walls are called secondary plasmodesmata (Ehlers & Kollmann 2001). The formation of secondary plasmodesmata allows cells to increase their potential for molecular trafficking and allows connections to be created between cells that are not related cytokinetically. As cells expand and differentiate, their fate determines the extent to which their cytoplasmic connectivity to other cells is maintained (Mezitt & Lucas 1996). Some cell types, such as those of the leaf mesophyll, remain closely connected to their neighbours, and may even lay down additional plasmodesmata to increase the continuity (Ding et al. 1992a). In other areas of the plant, for instance in vascular tissue, certain cells greatly reduce the number of plasmodesmata in their adjoining walls (Gamalei 1989). In this way, the cytoplasmic continuity can be altered depending on the tissue type (Botha & Evert 1988; Brown et al. 1995). However, although reductions in the number of plasmodesmata are common, only guard cells surrounding stomata (Erwee, Goodwin & van Bel 1985; Palevitz & Hepler 1985) and differentiating xylem elements (Lachaud & Maurousset 1996) lose all symplastic connections at maturity. In all other cells, some degree of intercellular connection is maintained. This plasmodesmal continuum that potentially exists throughout the whole plant is termed the symplast (Münch 1930). However, the symplast is not the open continuum that Münch originally hypothesized, but is divided into functional domains, each tightly regulated by different forms of plasmodesmata (Erwee & Goodwin 1985; Ehlers & Kollmann 2001). Plasmodesmata are now thought of as fluid, dynamic structures that can be modified both structurally and functionally to cope with the requirements of specific cells and tissues. Based on structure, two basic types of plasmodesmata have been characterized; simple and branched. Simple plasmodesmata consist of a single pore traversing the cell wall, whereas branched plasmodesmata have two or more channels on either side of the middle lamella, often joined by a central cavity. Electron micrographs of simple plasmodesmata are shown in Fig. 1A and B, and in diagrammatic form in Fig. 2. Simple plasmodesmata may be grouped together in primary pit fields and this form has been found to predominate in immature plant tissues (Oparka et al. 1999). Simple plasmodesmata are common in the lower plants such as algae and mosses (Franceschi, Ding & Lucas 1994; Cook et al. 1997) whereas branched plasmodesmata are found extensively in mature tissues and appear to represent more evolutionarily advanced structures (Lucas, Ding & van der Schoot 1993; Oparka et al. 1999). Both primary and secondary plasmodesmata are initially simple in structure but, during tissue development, may intrinsically form branches or fuse with neighbouring plasmodesmata to produce complex, branched structures. During the sink–source transition that occurs in leaves, simple plasmodesmata are gradually converted to branched plasmodesmata by a mechanism that involves the formation of bridges between adjoining simple pores (Fig. 2; see Oparka et al. 1999; Roberts et al. 2001). (A) Longitudinal section through simple plasmodesmata between adjacent vascular parenchyma cells in a mature sugarcane leaf. These plasmodesmata show constricted desmotubules and neck constrictions lacking sphincters. ER, endoplasmic reticulum. (Reproduced with permission from R.F. Evert and Planta; Robinson-Beers & Evert, 1991) Bar = 200 nm. (B) Transverse section through simple plasmodesmata between adjacent vascular parenchyma cells in a mature sugarcane leaf. The inner leaflet of the desmotubule appears as a central, electron-opaque dot. The cytoplasmic sleeve appears mottled due to the presence of electron-opaque, spoke-like extensions that extend from the oute