Plasmodesmata connecting companion cells (CC) to sieve elements (SE) are specifically modified to form specialised structures known as pore-plasmodesma units (PPU) (van Bel 1996) (Fig. 2d). The ER within these PPU
is believed to play a vital role in the survival of SE and functioning of the phloem. The SE-CC complexes form the functional units of phloem and are specialised for the long-distance flow of solutes. Both cells originate from an unequal division of the SE-CC mother cell. Soon after division, the plasmod-esmata on the CC side become highly branched, with up to 100 branches in some species (Evert 1990), coalescing in a central cavity that connects to a wider symplasmic pore at the SE side. It was previously reported that the ER was not continuous through the PPU, but it is now accepted that ER tubules traverse the PPU (Ding et al. 1993), although the ultrastructure of the central cavity has not as yet been resolved (van Bel and Kempers 1997). It has been suggested that branching of plasmodesmata occurs wherever the demand for symplasmic contact increases during development (Kollmann and Glockmann 1999; Ehlers and Kollmann 2001). If so, the asymmetric branching of the PPU implies the difference in permeability of the plasmodesmata on both sides of the cell wall (Schulz 2005).
During differentiation, selective autophagy results in the disintegration of most of the cellular components of the SE including the nucleus and vacuole. What remains at maturity is the plasma membrane, a thin layer of parietal cytoplasm composed of stacked ER or fenestrated ER (Thorsch and Esau 1981a,b; Sjolund and Shih 1983) and a few dilated mitochondria (Evert 1990). Phloem-specific plastids of two types, with proteinaceous (P-type plastids) or starch (S-type plastids) inclusions (Esau 1969; Behnke 1991a; van Bel and Knoblauch 2000; van Bel 2003), and SE phloem proteins (Eleftheriou 1990; Evert 1990; Cronshaw and Sabnis 1990; Behnke 1991b; Iqbal 1995) are also conspicuous in the SE. To prevent these organelles being dragged along in the turbulent mass flow within the SE, 7-nm-long macromolecular extensions anchor the ER, mitochondria and plastids to each other and to the plasma membrane (Ehlers et al. 2000). The resulting mature SE has been described as almost "clinically dead", and in many cases has to be maintained by the adjacent CC. The ER that is continuous from CC to SE is thought to provide a major "lifeline" for the trafficking of macromolecules that are essential to maintain the integrity of the SE (Oparka and Turgeon 1999; van Bel and Knoblauch 2000).
Compared to other organelles within the SE, the ER is well preserved in the form of nets or stacks (Thorsch and Esau 1981a,b; Sjolund and Shih 1983). The parietal fenestrated ER, which shares some traits with the cortical ER (Staehelin 1997), has been postulated to be a structural necessity for ATP-fuelled retrieval (Sjolund and Shih 1983), and may thus be essential for sucrose uptake and retrieval by the SE (van Bel 1996).
Attachment of macromolecules to the cytoplasmic face of the desmotubule has been proposed to allow the movement of proteins through the PPU connecting SE and CC (see Sect. 4.1 and Fig. 4). Due to the enucleate nature of SE and their lack of rough ER, it has been recognised that SE are dependent on CC for their functioning, in some cases for decades (Raven 1991). The flow rate within sieve tubes has been estimated to exceed 40 cm h-1 (Fisher 1990). If proteins or mRNA entering the SE via the PPU were simply "dumped" into the translocation stream, they would be swept rapidly away to sinks. This might be the case for some macromolecules, but it is likely that others are in some way anchored, particularly those required for the maintenance of the SE. It has been suggested that proteins or mRNA trafficked across a PPU remain bound to the desmotubule and subsequently move in association with the ER (Fig. 4). Such a process may occur following the targeting of the movement protein (MP) of Cucumber mosaic virus (CMV), fused to GFP, to PPUs.
Fig. 4 Schematic model depicting molecular trafficking between the CC and the SE. Left: Endogenous RNA molecules originating in the mesophyll are trafficked by specific molecular chaperones into the CC. At the PPU, the chaperone interacts with a receptor protein located on the desmotubule. In the case of some systemic RNA viruses, the viral RNA is trafficked into the CC by a specific viral movement protein (MP). As in the case of endogenous RNA chaperones, the MP interacts with the desmotubule to facilitate RNA movement into the SE. Other systemic viruses may traffic across the PPU as intact virions, without the need for disassembly in the CC. Right: Selective protein trafficking between CC and SE. Proteins synthesized within the CC and destined for the SE parietal layer are trafficked across the PPU by an interaction with receptor proteins located on the desmotubule. Such receptors ensure that the proteins are delivered along the ER to their target sites without loss to the translocation stream. After delivery, the receptor proteins may be recycled back into the CC to collect further cargo (arrows). Other low molecular weight proteins may enter the SE from the CC by diffusion. Such proteins may not possess "retention signals" for the ER, and may be translocated and unloaded in sink regions of the plant. (Adapted from Oparka and Turgeon 1999)
Upon entry into the SE, the MP trafficked along a reticular structure within the SE parietal layer (Blackman et al. 1998).
It is interesting to note that the cortical ER of higher plants is a highly dynamic system of tubules and sheets, and that this ER flow is probably driven by a close association with an underlying actin -myosin network (Boevink et al. 1998; Brandizzi et al. 2002). This raises the possibility that macro-molecules anchored on the cytoplasmic face of the cortical ER network might be delivered to the vicinity of plasmodesmata simply by random flow along ER membranes. Although the desmotubule is thought to be inserted into plas-modesmata from their inception, it is intriguing to speculate that in some circumstances the cortical ER might be able to physically move along actin filaments that traverse the plasmodesmal pore. In such a scenario, macro-molecules (including viral ribonucleoprotein complexes) might be able to "hitch a ride" on the mobile cortical ER system (Oparka 2004).
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