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Plasmodesmata and the Control of Symplastic Transport Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Publishing Ltd 2002 26 Original Article Plant, Cell and Environment (2003) 26, 103–124 Plasmodesmata and the control of symplastic transport A. G. ROBERTS & K. J. OPARKA Scottish Crop Research Institute, Invergowrie, Dundee, DD2 5DA, UK ‘There are holes in the sky other cells, some degree of intercellular connection is main- where the rain gets in, tained. This plasmodesmal continuum that potentially but they’re ever so small exists throughout the whole plant is termed the symplast that’s why rain’s so thin’ (Münch 1930). However, the symplast is not the open con- Spike Milligan (1968) tinuum that Münch originally hypothesized, but is divided into functional domains, each tightly regulated by different In 1879 Eduard Tangle discovered cytoplasmic connections forms of plasmodesmata (Erwee & Goodwin 1985; Ehlers between cells in the cotyledons of Strychnos nuxvomica, & Kollmann 2001). Plasmodesmata are now thought of as which he interpreted to be protoplasmic contacts. This led fluid, dynamic structures that can be modified both struc- him to hypothesize that ‘the protoplasmic bodies . are turally and functionally to cope with the requirements of united by thin strands passing through connecting ducts in specific cells and tissues. 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 func- THE STRUCTURE OF PLASMODESMATA tioned as autonomous units. It was after much research in Based on structure, two basic types of plasmodesmata have many other species and cell types that Strasburger, in 1901, been characterized; simple and branched. Simple plas- named these structures plasmodesmata (Carr 1976). modesmata consist of a single pore traversing the cell wall, During the division and differentiation of meristematic whereas branched plasmodesmata have two or more chan- cells, plasmodesmata are formed across each developing nels on either side of the middle lamella, often joined by a cell plate, allowing cytoplasmic and endomembrane conti- central cavity. Electron micrographs of simple plasmodes- nuity to occur between all daughter cells, and ultimately, mata are shown in Fig. 1A and B, and in diagrammatic form between all cells in a developing tissue (Mezitt & Lucas in Fig. 2. Simple plasmodesmata may be grouped together 1996). Those plasmodesmata that form during cell division in primary pit fields and this form has been found to pre- are termed primary plasmodesmata (Jones 1976). Those dominate in immature plant tissues (Oparka et al. 1999). that form de novo across existing cell walls are called sec- Simple plasmodesmata are common in the lower plants ondary plasmodesmata (Ehlers & Kollmann 2001). The for- such as algae and mosses (Franceschi, Ding & Lucas 1994; mation of secondary plasmodesmata allows cells to increase Cook et al. 1997) whereas branched plasmodesmata are their potential for molecular trafficking and allows connec- found extensively in mature tissues and appear to represent tions to be created between cells that are not related more evolutionarily advanced structures (Lucas, Ding & cytokinetically. van der Schoot 1993; Oparka et al. 1999). Both primary and As cells expand and differentiate, their fate determines secondary plasmodesmata are initially simple in structure the extent to which their cytoplasmic connectivity to other but, during tissue development, may intrinsically form cells is maintained (Mezitt & Lucas 1996). Some cell types, branches or fuse with neighbouring plasmodesmata to pro- such as those of the leaf mesophyll, remain closely con- duce complex, branched structures. During the sink–source nected to their neighbours, and may even lay down addi- transition that occurs in leaves, simple plasmodesmata are tional plasmodesmata to increase the continuity (Ding et al. gradually converted to branched plasmodesmata by a 1992a). In other areas of the plant, for instance in vascular mechanism that involves the formation of bridges between tissue, certain cells greatly reduce the number of plas- adjoining simple pores (Fig. 2; see Oparka et al. 1999; modesmata in their adjoining walls (Gamalei 1989). In this Roberts et al. 2001). way, the cytoplasmic continuity can be altered depending Due to the difficulty of isolating intact plasmodesmata on the tissue type (Botha & Evert 1988; Brown et al. 1995). from cell-wall fractions, structural models have tradition- However, although reductions in the number of plasmodes- ally been based on data from transmission electron micro- mata are common, only guard cells surrounding stomata graphs (Robards 1971; Robards & Lucas 1990; Beebe & (Erwee, Goodwin & van Bel 1985; Palevitz & Hepler 1985) Turgeon 1991; Ding, Turgeon & Parthasarathy 1992b; and differentiating xylem elements (Lachaud & Maurous- Botha, Hartley & Cross 1993; Overall & Blackman 1996; set 1996) lose all symplastic connections at maturity. In all Waigmann et al. 1997). Most models depict simple plas- modesmata as linear pores in the cell wall (Figs 1C & D), Plasmodesmata and symplastic transportA. G. Roberts & K. J. Oparka Correspondence: Alison G. Roberts. e–mail: [email protected] each lined by the plasma membrane, which is continuous © 2003 Blackwell Publishing Ltd 103 104 A. G. Roberts & K. J. Oparka Figure 1. (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 plas- modesmata 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 outer leaflet of the desmotubule toward the inner leaflet of the plasma membrane. (Reproduced with permission from R.F.Evert and Planta; Robinson-Beers & Evert, 1991) Bar = 100 nm. (C) and (D) Diagrammatic representation of the substructure of simple plasmodesmata in longitudinal (C) and transverse (D) sections. ER, endoplasmic reticulum; CW, cell wall; CS, cytoplasmic sleeve; D, desmotubule; CR, central rod; PM, plasma membrane; SP, spoke-like extensions; PMP, plasma membrane-embedded proteins; DP, desmo- tubule-embedded proteins. (Based on model in Ding et al. 1992b). between adjacent cells. In the centre of the pore lies a ture with an internal lumen, whereas Tilney et al. (1991) strand of modified cortical endoplasmic reticulum, the des- speculated that it exists as a solid, proteinaceous rod. The motubule (Robards & Lucas 1990; Ding et al. 1992b; Lucas desmotubule has been found in both an appressed and & Wolf 1993; Epel 1994). Different structural models of the dilated state (Overall, Wolfe & Gunning 1982; Robinson- desmotubule have been postulated. Gunning & Overall Beers & Evert 1991; Waigmann et al. 1997). (1983) showed it to have a cylindrical, membranous struc- It is thought that most endogenous cytoplasmic mole- © 2003 Blackwell Publishing Ltd, Plant, Cell and Environment, 26, 103–124 Plasmodesmata and symplastic transport 105 Figure 2. Diagrammatic representation of the structural change from simple to branched plasmodesmata. During development, the simple pore develops into a complex, branched structure with a central cavity aligned along the middle lamella of the cell wall. This transformation occurs via an H-shaped intermediate that appears to form by the introduction of a new protoplasmic bridge between neighbouring pairs of simple plasmodesmata. WC, wall collar; CW, cell wall; ML, middle lamella; D, desmotubule; PM, plasma membrane; ER, endoplasmic reticulum; CC, central cavity. (Re-drawn from Oparka et al. 1999) cules, and plant viruses, utilize the cytoplasm between the (Robinson-Beers & Evert 1991; Waigmann et al. 1997). desmotubule and plasma membrane, a region known as the Very little is currently known about the proteins that con- cytoplasmic sleeve (Esau & Thorsch 1985), to move from tribute to the structure of plasmodesmata, and many, if cell to cell (Lucas & Wolf 1993; Epel 1994; Kragler, Lucas not most, plasmodesmal proteins await isolation and & Monzer 1998a). However, trafficking between cells via functional characterization. the desmotubule has also been reported (Cantrill, Overall & Goodwin 1999). At both ends of the plasmodesma, in TRANSPORT VIA THE CYTOPLASMIC SLEEVE the neck region, the channel is frequently constricted (Fig. 1A), and the cytoplasmic sleeve may be partially Transport of many small molecules through plasmodesmata occluded with globular subunits. The subunits are thought occurs via the cytoplasmic sleeve. Passively loaded fluores- to exist in a helical arrangement that may functionally cent probes (Duckett et al. 1994; Roberts et al. 1997) and divide the space into a number of spiralling channels (Zee microinjected dyes (Goodwin 1983; Erwee et al. 1985; 1969; Robards 1976; Olesen 1979; Overall et al. 1982; Wolf Madore & Lucas 1986; Oparka et al. 1991) utilize this path- et al. 1989; Olesen & Robards 1990; Robards & Lucas 1990; way, and larger molecules, including green fluorescent pro- Ding, Turgeon & Parthasarathy 1991; Robinson-Beers & tein (GFP; see below) may also move via the cytoplasmic
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