FEATURE ESSAY 10.1 Communication between plant cells

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Robyn Overall

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Figure 1 Robyn Overall, School of Biological Sciences, University of Sydney

 Individual plant cells communicate directly with one another through minute membrane-lined channels — plasmodesmata — which traverse the cell wall. Other less direct forms of communication orchestrate the coordination of growth and development of an individual cell with that of its neighbours. Without such coordination, plant growth would be like the disorganised growth of a callus in a tissue culture. I have derived much joy from my adventures trying to understand what mechanisms individual cells use to communicate with one another and more indirectly to coordinate their growth.

Electric fields as coordinators of plant growth?

After graduating with my PhD, I became fascinated by Lionel Jaffé’s demonstrations that plants and animals generate steady electric fields around themselves. These fields are maintained by a steady flow of ions due to asymmetric distribution of ionic leaks and pumps in the plasma membrane. During the late 1970s and 1980s, much activity and excitement culminated in the suggestion that electric fields may play a role in establishment of polarity, regeneration after wounding and initiation of new growth axes, whether a limb bud or a branch. I spent two years with Lionel Jaffé at Purdue University, USA, measuring electric currents around Drosophila oocytes during establishment of the polarity that ultimately governs the whole organism’s development.

A plant biologist at heart, I wondered if these self-generated electric fields might also orchestrate growth and development of individual plant cells, allowing coordination of organised plant tissues. Certainly electric fields had been measured around higher plants since the 1930s by Lund in Texas and the 1950s by Scott in Tasmania. Crucially, the electric field was always parallel to the direction of organ expansion, and any change in growth direction, such as initiation of a lateral root or regeneration following wounding, was preceded by a local reorientation of the field to become parallel to the new direction of growth. On returning to ANU and then Sydney University, I put together the equipment for measuring minute electric currents. Through many collaborators and research students, we demonstrated fields around somatic embryos in tissue culture, during wounding in pea roots, and during incipient development of buds in Graptopetalum.

If electric fields are a key to growth coordination, then what is the mechanism? One obvious manifestation of devel-opment of individual cells is the direction of expansion leading to particular cell shapes. Direction of expansion is determined by the net orientation of the most recently deposited cellulose microfibrils, and orientation of these, in turn, is dictated by the orientation of cortical microtubules within the cell. The direction of expansion is parallel to the direction of the innate electric field so the microtubules should lie perpendicular to the field direction. Indeed, we confirmed this in wounded pea roots, showing microtubule reorientation around the wound site after 5 h perpendicular to the large wound currents. Most remarkably, microtubule orientation appears to transcend cell boundaries, implying a communication between adjacent cells, and responds to a single orienting vector. Likewise, applied electric fields reorient microtubules and can bring about coordinated growth in callus.

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Figure 2 Large molecules can pass from cell to cell. Here, fluorescently labelled dextran, a membrane-impermeant polysaccharide of about 10 kDa in size, was micro injected into a living stem epidermis cell of Torenia fournieri. Thirty seconds later, movement of label into some adjoining cells, presumably via plasmodesmata, is clearly visible as fluorescing nuclei and cytoplasm. The red-orange fluorescence of guard cells is from their chloroplasts. Scale bar = 25 μm.

(Photograph courtesy L.C. Cantrill, P.B. Goodwin and R.L. Overall; reproduced with permission of Elsevier Science)

Unravelling the mysteries of plasmodesmata

Professor Brian Gunning introduced me to plasmodesmata during my PhD at ANU in the 1970s. My passion to unravel their secrets has led me and my group to use a wide variety of techniques. We have developed electrophysiological procedures in which fine-tipped glass needles are inserted into adjacent cells and the electrical resistance of plasmodesmata calculated from the voltages recorded when a pulse of electric current is injected into one of the cells. With this technique we have demonstrated that plasmodesmata can open and close rapidly, within seconds. We have injected fluorescently tagged molecules of different sizes to show that the size of molecules that can pass from cell to cell varies during development (Figure 2). Details of plasmodesmata structure have been difficult to obtain because their diameter (50 nm) is smaller than the thickness of a thin section for electron microscopy and their configuration appears to be altered by the very processes needed to observe them. However, using antibodies which bind to known proteins, we have discovered that the cytoskeletal components actin and myosin are components of plasmodesmata. The next step is to isolate proteins specific to plasmodesmata.

The challenge then is to combine results from these diverse techniques to generate a working model for the mechanism of transport and its regulation through plasmodesmata. Over the last 30 years, a number of models of plasmodesmata have been put forward largely on the basis of interpretation of images from electron microscopy and inferences about the mode of transport through them. On reflection, what were often put forward as speculative working models by their authors have then been unquestioningly taken on by others as experimentally proven fact. It is still to be established what the exact role of the cytoskeleton is in plasmodesmata, although it is tempting to speculate that it is involved in the regulation of their permeability or the trafficking of large molecules through them. It may even be that the coordination in growth discussed above is mediated by direct cytoskeletal links between adjacent cells.

Plant viruses are known to facilitate their own spread through plasmodesmata through the production of a ‘movement protein’ which increases the size of molecule that can normally pass through these channels. Nothing is known of how this movement protein interacts with plasmodesmata, although we have identified structures around the necks of plasmodesmata which are likely candidates for modulators of their dimensions. It is an exciting possibility that identification of the details of this interaction could be a fundamental step in the generation of viral-resistant plants. At the outset of my efforts with the basic biology of plasmodesmata, it was far beyond my imagination that the work could eventually play a role in the solving of a practical problem of such vast economic importance!

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