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Plasmodesma Are the Key South Afrtcan Journal of Botany 2001. 67 I • 9 Copynglll tSJ NISC Pty Ltd Prtnted m Sot~II! Afnca -All nghts reserved SOUTH AfRICAN JOURNAL Of BOTANY ISSN 0254-6299 Mini review Regulation within the supracellular highway - plasmodesma are the key CEJ Botha'* and RHM Cross2 ' Botany Department and 2 Electron Microscopy Unit, Rhodes University, Grahamstown 6140, South Africa * Corresponding author; e-mail: [email protected] Received 16 October 2000, accepted in revised form 19 October 2000 Plasmodesma! connections are unique, highly dynamic intercellular passages and connections. With time, intercellular structures that are lined by the plas­ these connections have evolved to allow some degree mamembrane. They are believed to be a vital intercellu­ of regulation and traffic control. This paper explores lar communication channel between living cells, linking some of the structure/function relationships in plas­ numbers of living cells into interconnected, highly spe­ modesmata. Attention is focused on the potential role of cialised cellular domains, thus enabling the plant to act the neck region of these remarkable structures and dis­ as an integrated organism. Their evolution in the higher cusses models which may explain the processes plant was inevitable. It is .accepted that cell heterogene­ involved in regulating the movement of substances ity rather than cell divergence pressurised developing from cell to cell. plant systems along a route that led to the formation of Introduction Plasmodesma are unique intercellular cytoplasmic commu­ based microinjection techniques have allowed these tech­ nication channels that traverse the walls between living plant niques to be applied in a number of study programmes cells. Within the limiting tubule formed by the plasmamem­ (Schulz, 1999 and references cited) including real-time brane, which traverses the common wall between living observation of injection of fluorescent probes into living cells, the endoplasmic reticulum joins the adjacent cells cells. This new dimension has provided answers to some through the plasmodesma in a highly-modified ER stru cture, important, yet fundamental questions relating to intercellular called the desmotubule. The desmotubule is separated from trafficking (see Botha and Cross 1997, Botha and Cross the inner leaflet of the plasmalemma by a space that is 2000, Botha et at. 2000). Table 1 summarises some of the termed the cytoplasmic sleeve . It is the cytoplasmic sleeve concepts associated with the structure and function of plas­ which is believed to be involved in the direct cell-to-cell traf­ modesma. ficking process. Plasmodesma have diverse functions and it seems that they are capable of trafficking a large variety of Trafficking and transport processes molecules and signalling structures, of widely differing molecular mass. We recognise that substances are able to move through The movement of substances through the transport sys­ adjacent cells, following a pathway that is entirely contained tems in plants has occupied the attention of plant scientists by living interconnected protoplasts, collectively termed the for nearly 150 years. Improvements in technologies such as symplasm. In contrast, the apoplasm, defined as that region microscopy and microinjection have allowed more refined of the plant not bounded by the plasmamembrane, also is observations on cell-to-cell communication processes, and involved with energy-free short- and long-distance transport have allowed us to focus on regulation and control mecha­ in plants. The existence of two transport systems means that nisms within the processes involved. division of labour is possible, but, at the same time, compli­ Given the strong interrelationship between plant structure cates the transport processes within large supracellular and function , It is not surprising that many researchers organisms. It cannot be disputed that the symplasmic path­ remain focussed on the leaf and. in particular, the process­ way (in this context, the phloem) is highly dependent upon es that govern uptake and transport of assimilates and relat­ the apoplasmic pathway (the xylem) for a steady supply of ed materials. These interests remain concentrated at the water, without which little if any symplasmic transport microstructural and physiological levels. Exciting advances through the complex higher plant supracellular organism made in the past decade in light and confocal microscope- would be possible. How are these two contrasting, but com- 2 Bolha and Cross plementary pathways and specifically, their contents kept are at the heart of cell to cell traffic control and regulation separate from each other? Are there control points and if so (Marchant 1976, Lucas eta/. 1993, Bergmans eta/. 1997, how does the plant maintain a normal functional physiologi­ Jane and Chiang 1993, Eleftheriou 1993, Franceschi el a/. cal state? Clearly, the interactivities between these systems 1994, Vasil'ev 1997). Plasmodesma! permeability is an will result in a balanced and finely tuned transport system active business (Pickard and Beachy 1999) in which mes­ that can be regulated at several points. sengers such as IP3 and ca++ participate in the control of Cell to cell transport is a complexity of processes - each permeability. interacting or acting in solitude to produce a potential cas­ cade controlling mechanism. Water loss and carbohydrate Plasmodesma. meristems, domains and field transfer must be interlinked within the whole plant; other­ boundaries wise, an unorchestrated discordant system will exist. The loading of assimilates must therefore be complex, involving Convergent evolution amongst divergent taxa may well tell a series of cell-to-cell short distance transfer processes via us something about plasmodesma! evolution. Cook and plasmodesma. These are coupled with a freer apoplasmic Graham (1999) suggest that there is a clear correlation water transfer from the xylem to the cell walls and intercel­ between the ability to form plasmodesma and the ability to lular spaces of the mesophyll, as well as into the cytoplasm form meristematic tissue (van der School and Rinne 1999a). of the mesophyll and surrounding tissues. In grasses, part of Previously, Jian eta/. (1997) conducted a series of experi­ the overall ph loem loading controlling mechanism may be ments which demonstrated that there were changes in the found at the junction between the bundle sheath (BS) and ultrastructure, as well as in the subcellular localisation of the mesophyll (MS). It is at the MS- BS interface where ca++ in poplar (Populus deltoides Bartr. ex Marsh) apical many species regulate outward water loss and inward car­ bud cells during the induction of dormancy by short-day (SO) bohydrate uptake. Regulation of the outward loss of water photoperiods. These authors reported an increase in the can be undertaken by the suberin lamella (Botha and Evert number of starch granules, as well as a significant accumu­ 1986 and literature cited), which may force adoption of a lation of vacuolar storage proteins in the apical bud cells. more regulated symplasmic pathway through plasmodesma Coupled with this , they observed constriction and blockage at this interface. Internal to the bundle sheath, three alterna­ of the plasmodesma. These results suggest that under the tive phloem-loading pathways exist - along entirely sym­ influence of SO photoperiods, there are alterations in sub­ plasmic or apoplasmic pathways, or via a mixed mode sym­ cellular Ca-2+ localisation. and changes in ultrastructure of plasmic-apoplasmic pathway. Clearly, there are many plants apical bud cells during the development of dormancy. The where phloem loading occurs via a mixed pathway (refer­ constriction and blockage of plasmodesma it seems, may ences cited in Botha and Cross 1997). cause the cessation of symplastic transport, limit cellular Undoubtedly these important, yet diverse transport super­ communication and signal transduction between adjacent highways remain the subject of significant and directed cells. This in turn, may lead to even ts associated with growth research, and there are now obviously defined focus areas cessation and dormancy development in buds. which are being actively pursued in a number of laboratories Thus, complex cellular interactions, which require the worldwide. The re-focussing of ideas has come about as a exchange of morphogenetic signals, underlie the process of result of the aforementioned applica tion of advances in light morphogenesis within shoot apical meristems (Rinne and and electron micrography, particularly those using fluo­ van der School 1998, 1999b). It has been suggested that all rophores, and coupled with this, the rapid improvements in apical meristem cells are interconnected by plasmodesma confocal microscopy which have contributed a great deal to and thus could be subject to regulation, especially during the rekindling of 'old' interests and. significantly, in some new cell division cycle (Ehlers and Kollmann 1996). Rinne and discoveries (Knoblauch and van Bel 1998). van der School (1998) were able to demonstrate that two Many of the new ideas associated with intercellular traf­ concentric fields exist in the apical meristem of Betula ficking in plants are encompassed in the work published pubescence, which effectively restricts the symplasmic diffu­ recently by van Bel, Gunther and van Kesteren (1999), who sion of small morphogens to the cells within the boundaries state that there is widespread opinion that the evolution of of their
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