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Plasmodesmata: Composition, Structure and Trafficking Plant Molecular Biology 26: 1343-1356, 1994. © 1994 Kluwer Academic Publishers. Printed in Belgium. 1343 Plasmodesmata: composition, structure and trafficking Bernard L. Epel Botany Department, Tel Aviv University, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel Received and accepted 13 September 1994 Key words: conductivity, movement, plasmodesmata, size exclusion limit, proteins, viruses Abstract Plasmodesmata are highly specialized gatable trans-wall channels that interconnect contiguous cells and function in direct cytoplasm-to-cytoplasm intercellular transport. Computer-enhanced digital imaging analysis of electron micrographs of plasmodesmata has provided new information on plasmodesmatal fine structure. It is now becoming clear that plasmodesmata are dynamic quasi-organelles whose con- ductivity can be regulated by environmental and developmental signals. New findings suggest that sig- nalling mechanisms exist which allow the plasmodesmatal pore to dilate to allow macromolecular transport. Plant viruses spread from cell to cell via plasmodesmata. Two distinct movement mechanisms have been elucidated. One movement mechanism involves the movement of the complete virus particle along virus-induced tubular structures within a modified plasmodesma. Apparently two virus-coded movement proteins are involved. A second movement mechanism involves the movement of a non-virion form through existing plasmodesmata. In this mechanism, the viral movement protein causes a rapid dilation of existing plasmodesmata to facilitate protein and nucleic acid movement. Techniques for the isolation of plasmodesmata have been developed and information on plasmodesma-associated proteins is now becoming available. New evidence is reviewed which suggests that plasmodesmatal composition and regulation may differ in different cells and tissues. Introduction Plasmodesmata were thought for many years to be nonselective pores, passively allowing the In higher plants, cell-to-cell communication as bi-directional movement of molecules between well as nutrient transport may be symplastic, via adjacent cells. During the past few years this static junctional structures called plasmodesmata or concept of the plasmodesmata has been changing apoplastic, via membrane-associated receptors, and it is now clear that plasmodesmata are dy- trans-membranous gatable channels and/or namic selective entities with the capacity to 'gate'. transporters. Plasmodesmata are highly special- Evidence is now emerging which suggests that ized gatable cytoplasmic trans-wall channels plasmodesmatal composition and regulation may that interconnect contiguous cells and function in differ in different cells and tissues. In this review, the direct cytoplasm-to-cytoplasm intercellular we consider new studies on plasmodesmatal movement of water, nutrients, small signalling structure, composition, on the regulation of gat- molecules and, in certain cases, of macromol- ing, and on virus-induced alterations in plas- ecules. modesmatal conductance. [107] 1344 Plasmodesmatal structure (PERC). It is entirely conceivable that within the plasmodesmata the ER has undergone major Early electron micrography studies ofplasmodes- modifications, and that different parts of the plas- mata led to a simple general consensus model modesmatal ER component have different com- describing the plasmodesma as a wall-embedded positions. plasmalemma-lined unbranched cylinder that The substructural detail of plasmodesmata in contains a central axial component generally higher plants has been examined by various termed the desmotubule. For a review of early workers and a number of models have been pro- structural aspects of plasmodesmata, see the book posed (see review by Robards and Lucas [ 55 ]; [ 7, by Gunning and Robards [29]. The desmotubule 14, 68]). Recently, two models ofplasmodesmatal was considered to be derived from and continu- structure were proposed based on computer- ous with the endoplasmic reticulum of adjoining enhanced digital imaging analysis of electron mi- cells. Recent studies suggest that the endoplasmic crographs of plasmodesmata from a dicotyledon- reticulum (ER) component of a plasmodesma is ous plant [14] and from a C4 grass [7]. a derivative of and continuous with cortical ER Ding et al. [14] examined the substructure of [30, 31, 52]. In some cells, the outer regions of the the plasmodesmata of the C3 dicot Nicotiana plasmodesma are constricted and form what has tabacum following cryofixation and freeze substi- been termed the neck region, a structure which is tution. According to their model, the plas- not a general feature of all plasmodesmata [56]. modesma is depicted as a complex pore-contain- The cylindrical space between the desmotubule ing proteinaceous particles embedded in the inner and the plasmalemma has been referred to as the leaflet of the plasma membrane and in the outer cytoplasmic annulus or sleeve. Most models con- leaf of the desmotubule. Spoke-like filamentous sider the cytoplasmic annulus as the pathway strands apparently connect the globular proteins through which transport occurs. Electron micro- of the outer leaf of the desmotubule to the pro- graphs show that in the orifice region, the ER was teins embedded in the encasing PD plasma mem- apparently constricted and no lumen was de- brane. The central region of the desmotubule, the tected. Lucas et al. [38] have suggested that, since so-called rod, an electron-dense region, is de- it is now clear that the desmotubule is not a tu- picted as being composed of a series of particles, bule but a modified ER, its nomenclature should probably protein, that are embedded in the lipid be changed to appressed ER. This new nomen- of the fused inner leaflet of the ER membrane. In clature may not be appropriate for a number of their model, the desmotubule is constricted and reasons. The term 'appressed' refers to laminar no lumen is present. It was suggested that the structures while the ER within the plasmodesma electron-dense particles embedded in the inner is more like a cylinder. A more appropriate de- leaflet of the plasmalemma and the outer leaflet of scriptive term might be constricted ER rather than the desmotubule form a convoluted channel that appressed ER. Furthermore, within the more in- functions as a molecular sieve, determining the terior regions of the plasmodesmata, the ER often size exclusion properties. It was further hypoth- balloons and a lumen is present, i.e. it is neither esized that the radial spokes may function in dy- appressed or constricted. Most importantly, we namically altering the effective radius of the cy- feel that one must be cautious in interpreting static toplasmic sleeve, thus regulating the size exclusion electron micrographs. The ER within the plas- limit of the plasmodesma. modesmatal channel may be a dynamic structure, Botha et al. [7] employed similar computer en- constricting and dilating as signalling and func- hancement techniques with plasmodesmata at the tion dictate. We feel that the term 'desmotubule' Kranz mesophyll bundle sheath interface of Ther- could be retained. However, if one feels the meda trianda, a C4 grass. Their model showed need to use a functional neutral term, then one many similarities to that of Ding et al. [ 14] but can refer to the 'plasmodesma ER component' with a number of significant differences. Associ- [108] 1345 ated with the inner plasmalemma leaflet and the limit (SEL) and selectivity of plasmodesmata. outer desmotubule wall were particles ca. 2.5- These new studies indicate not only that the plas- 3 nm in diameter, presumably proteins that abut- modesma can be gated, but that the size exclusion ted into the so-called cytoplasmic sleeve. In the limit can be modulated by environmental and de- central region of the desmotubule were electron- velopmental signals. dense particles also about 2.5 nm in diameter. In The diffusion selectivity of plasmodesmata to a contrast to Ding et al. [14], Bothe et al. [7] de- series of fluorescein labelled probes was re- tected the presence of a lumen of about 2.5 nm in examined quantitatively by Tucker and Tucker diameter between the central protein core and the [73] employing fluorescein labelled (F-) mono-, desmotubule wall. Furthermore, filamentous con- di-, tri- and quatra-amino acids. Their data sug- nections were observed between the central rod gested that the plasmodesmata of the stamenal particles of the desmotubule and the desmotubule hairs of Setcreasea purpurea have a size exclusion wall. This was in contrast to the model of Ding limit of about 800 Da and select for small hydro- et aL [ 14] for the plasmodesma for N. tabacum, in philic molecules with a charge from -2 to -4. which the spoke-like filamentous strands con- Molecules, however, that have attached aromatic nected proteins of the outer leaf of the desmotu- amino acid such as phenylalanine and tryptophan bule to the proteins embedded in the encasing PD exhibited low mobility and their kinetic curves, as plasma membrane. The data and model present well as those of F-(meth)2 and F-(his)2 generally by Bothe et al. [7] brings into question the gen- did not fit simple diffusion kinetics. When car- eral consensus that desmotubules are constricted boxyfluorescein (CF), a highly mobile probe was and can not function in cell-to-cell transport. Ad- micro-injected into the cytoplasm of cells previ- ditional studies are needed to address this ques- ously micro-injected with probes whose transport tion. was apparently
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