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The Role of Cytoplasmic Streaming in Symplastic Transport Blackwell Science, LtdOxford, UK PCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2002 26 845 Role of cytoplasmic streaming in symplastic transport W. F. Pickard 10.1046/j.0016-8025.2002.00845.x Original ArticleBEES SGML Plant, Cell and Environment (2003) 26, 1–15 The role of cytoplasmic streaming in symplastic transport W. F. PICKARD Department of Electrical Engineering, Washington University, St Louis, Missouri 63130, USA ABSTRACT effectuators. In the context of the cell, which participates in a far more decentralized command structure than an army, The distributing of materials throughout a symplastic this means: (i) carrying out its programmed activities; (ii) domain must involve at least two classes of transport steps: sensing its surroundings and its internal state and transmit- plasmodesmatal and cytoplasmic. To underpin the latter, ting appropriate information and/or commands; and (iii) the most obvious candidate mechanisms are cytoplasmic receiving and effecting commands from elsewhere in the streaming and diffusion. The thesis will be here advanced plant. that, although both candidates clearly do transport cyto- None of this is simple. and all of this must be done in a plasmic entities, the cytoplasmic streaming per se is not of complex three-dimensional ultrastructural milieu which primary importance in symplastic transport but that its does not conform to the diffusion-dominated ‘watery bag’ underlying molecular motor activity (of which the stream- model of yesteryear (Hochachka 1999). To paraphrase the ing is a readily visible consequence) is. Following brief tuto- elder Moltke, ‘in [physiology] with its enormous friction rials on low Reynolds number flow, diffusion, and targeted even the mediocre is quite an achievement’ (van Creveld intracytoplasmic transport, the hypothesis is broached that 1985, p.13). Or to cite from Polybius (a soldier/historian of macromolecular and vesicular transport along actin track- the 2nd century BC) a rather more direct parallel between ways is both the cause of visible streaming and the essential war and biology: ‘nature makes a single trivial error suffi- metabolically driven cytoplasmic step in symplastic trans- cient to cause failure in a design, but correctness in every port. The concluding discussion highlights four underdevel- detail barely enough for success’ (van Creveld 1985, p. 264). oped aspects of the active cytoplasmic step: (i) visualization That the plant fares very well indeed speaks volumes for of the real-time transport of messages and metabolites; (ii) the robustness and resilience of its strategies. enumeration of the entities trafficked; (iii) elucidation of In the distribution of both supplies (logistics) and infor- the routing of the messages and metabolites within the mation (C3) the plant has many options, including: cytoplasm; and (iv) transference of the trafficked entities from cytoplasm into plasmodesmata. 1 Convection. This form of mass transport is, in plant biol- ogy, typified by cytoplasmic streaming. If the supplies are Key-words: cytoplasmic streaming; diffusion; endoplasmic metabolites, they will certainly be carried along by the reticulum; intracellular transport; molecular motors; motion of the cytoplasm. If the information is encoded in plasmodesmata; trafficking. chemical messengers, it too will be carried along by the motion. However, the transport will be only along the streamlines of the flow: convection will never move INTRODUCTION metabolites or chemical messengers perpendicular to the flow. Convection is presently considered to be a result of The green plant, like an army, has two all-consuming activ- endoplasmic ‘molecular motors’ running along actin ities, without which it can not hope to prevail. The first of microfilaments or possibly along microtubules (Reddy these is logistics. The second is command, communication, 2001). But it is an open question whether the convective and control (C3). Because the topic of this is essay cytoplas- flow (i) constitutes a major payoff arising from this mic (protoplasmic) streaming in the context of symplastic motile activity; or (ii) is a byproduct of lesser utility transport, these two imperatives will be treated in the con- which arises from drag on the entities towed by the mov- text of a cell whose contents are convecting. ing motors. That is, how is the utility to the cell of motor Logistics is the art/science of getting the supplies needed motion to be apportioned between (a) stirring of the to the unit (a cell) and distributing them appropriately. in cytoplasm; and (b) siting of the towed entity at a new the context of the cell. This means: (i) taking them up, location; presumably a cost function exists and is either across the plasmalemma from the apoplast or from reflected by plant evolution, even though we do not at the protoplasm of a neighbouring cell by way of connecting present know how to formulate it. plasmodesmata; and (ii) distributing them appropriately 2 Diffusion. This reflects the kinetic motion of the mole- within the protoplasm. Our focus will be upon distribution. cules comprising the cytosol. As a result of intermolecu- C3 is the art/science of gathering reliable information lar collisions, a molecule in a particular compartment of and then transmitting unambiguous orders to appropriate the cytosol will execute a random walk and will, other Correspondence: William F. Pickard. Fax: +1 314 935 7500; influences being absent, tend in time to assume a uniform e-mail: [email protected] probability distribution within the compartment (cf. Saha © 2003 Blackwell Publishing Ltd 1 2 W. F. Pickard & Srivastava 1950 and van Kampen 1981). Diffusion can tinuum. The symplast is cytoplasmic; the apoplast is the cell move metabolites and messengers perpendicularly to the wall and beyond. But somehow, in common usage, ‘sym- streamlines of cytoplasmic flow. plastic transport’ only peripherally includes transport in the 3 Tow. This denotes a motive force imposed differentially phloem. Perhaps an adequate way of putting it is: upon certain classes of entities in a medium. For example, ‘Symplastic transport’ denotes the transport and distribu- the motion of electrons and holes in a semiconductor is a tion of molecules in general and chemical messengers in ‘tow’ phenomenon called drift. Magnetophoretic sedi- particular within the cytoplasm of a symplast domain of mentation of amyloplasts by a non-uniform magnetic nonvascular cells and the spreading of these molecules field (e.g. Kuznetsov & Hasenstein 1996) is likewise a from cell to cell via plasmodesmata’. ‘tow’ phenomenon; and so also would be selective cou- pling of myosin to some particular type of macromole- The concept of ‘symplast domain’ is well discussed by cule (or vesicle) and the subsequent translocation of the van Bel & Oparka (1995). macromolecule along actin trackways. Obviously, when Moreover, the apoplast no longer appears as inert and the towed entities are dragged through a fluid, convec- uninteresting as it once did and is increasingly implicated in tion will result. Obviously also, tow may be mediated storage, transport, and reactions (cf. Sattelmacher 2001). In either by fields (‘action at a distance’) as in sedimentation addition, although the bulk of the mole-miles racked up and magnetophoresis or by direct mechanical linkage as in symplastic transport must occur in the cytoplasm, yet in molecular motor based processes. nevertheless satisfactory transport still depends vitally 4 Electrical. This could be electrophoretically driven mass upon such processes as trans-plasmalemmal water flux, flow, but there is little evidence that this is important on plasmodesmatal function, and phloem transport. That is, an intracellular level; and, were it to exist, it should be long-distance transport in plants must be viewed as an inte- highly wasteful of metabolic energy because the cyto- grated system-wide problem of logistics in which issues of plasm is very close to electrical neutrality (cf. Pickard command and control are unavoidable, even if not clearly 1965). Or it conceivably might be electrically mediated understood at present. information transfer, except that long-distance nerve-like signalling is uncommon in plants and intracellular infor- mation transfer by electrical means has not been shown CONVECTION: MASS FLOW AT LOW to exist (e.g. Pickard 1973; 2001). REYNOLDS NUMBER 5 Pressure. On the whole plant level this could include sig- nals such as pressure disturbances (Malone 1996). On the Convection within the cytoplasm is called ‘cytoplasmic cellular level, the focus of this review, this could be man- streaming’ (or ‘protoplasmic streaming’); and its discovery ifested either by pole-to-pole pressure driven mass flow is attributed to Bonaventura Corti (e.g. Pfeffer 1906, coupled to plasmodesmata or by transcellular osmosis; as Kamiya 1959). It has been reviewed repeatedly, for exam- this possibility has not been extensively studied, it will be ple by Ewart (1903), Pfeffer (1906), Kamiya (1959, 1960, largely neglected. 1981), Britz (1979), Seitz (1979), Kuroda (1990), Shimmen & Yokota (1994), Grolig & Pierson (2000), and Staiger This leaves the first three items of the list as the prime can- (2000). didates for mediating the steps of symplastic transport That streaming in the plant cell is of key importance which occur within an individual cell. They will be discussed is graphically borne out by the classical observation one by one in subsequent sections. (Hofmeister 1867; Fig. 10) that, if some care is taken, a cell But before
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