FACTS AND MECHANISMS: A COMPARATIVE SURVEY

Abstract

Summary: 1. This review aims to survey the process of translocation of solutes in the phloem, including the experimental observations of the process, hypothetical mechanisms with their consequences, and the compatibility of these mechanisms with the experimental information.2. Some properties of the sieve elements are summarized. The characteristic constituent of the sieve elements is a fibrillar protein, P‐protein, of 60–120 A. filaments, whose function and distribution in intact sieve elements are still the subject of debate.3. Apart from the very high levels of sucrose (0.3–0.9 m) and of specific amino acids and amides (10–100 mm), the contents of the sieve elements are characterized by close regulation of the ionic content; thus K (20–85 ^mM) and Mg (2.3–23 mM) are very high relative to Na (0.06–0.3 mM) and Ca (0.25–0.5 mM) respectively; the pH is also very high.4. Convective movement (mass flow) is demanded by the very high rates of mass transfer. The longitudinal sucrose flux is about 2.5 times 10⁶ pmoles cm.^‐2 sec.^‐1 in petioles, and several times higher in fruits or trees; this is about 10⁵ times any reasonable transmembrane flux, and demands very large loading areas for each file of sieve elements. It also renders unlikely any mechanism demanding an associated trans‐membrane flux of any solute which approaches within several orders of magnitude of the sucrose flow.5. The evidence from tracer measurements (of ¹⁴C or of heat) favour a mass flow of some kind in the sieve tube, with only restricted exchange between the flowing stream and other sucrose pools in the phloem (or out of it). It is not consistent with ready equilibration with a large stationary reservoir of sucrose, or with reverse flows. There is close correspondence between the input and output kinetics of a length of the trans‐location path, or of build‐up curves at different distances; hence lateral exchange from the moving stream is relatively minor.6. Tracer measurements show that loading into the translocation stream is relatively slow, and is the main determining factor in the time course of appearance of tracer down the stem, or in the profile of radioactivity against distance in the stem. This applies not only to the initial steep front of radioactivity in the stem, but also to the error function profiles found at longer times in some plants; those do not arise as has been suggested, by exchange in a two‐way system of transcellular strands, but are a reflexion of the loading kinetics.7. The evidence for or against bidirectional movement is equivocal. In conditions in which there is a strong source/sink gradient imposed, the movement of both labelled carbon and heat is consistent with a one‐way system, and is difficult to reconcile with two‐way movement. However, in the absence of any strong gradient there is evidence for bidirectional movement. It is suggested that the pattern of flow, as well as the direction and rate of flow, may be controlled by the source/sink relations along the path.8. Electro‐osmosis as a mechanism for translocation seems to be ruled out by a number of theoretical difficulties. The most basic of these is the fact that an electro‐osmotic mechanism is inherently incapable of the transport of both anions and cations, whereas the phloem can do both. There are further quantitative difficulties. The ratio of sucrose to potassium in the sieve elements is about 10, and if potassium provides the current a longitudinal potassium flux of about 2.5 times 10⁶ pmoles cm.^‐2 sec.^‐l would therefore be required in petioles, and considerably more in fruits or trees. This raises very great difficulties of potassium circulation to provide a complete current loop, in the path of recirculation, the size of the transmembrane fluxes required, and the energetics of pumping enough potassium to maintain the driving force for electro‐osmosis.9. Possibilities of activated mass flow, by a mechanism similar to that involved in protoplasmic streaming are discussed. Experimental work on streaming in Nitella and in the slime mould Physarum is reviewed, including the evidence that in both these systems, fibrils, made up of 50–70 Å. filaments, are responsible for the production of the motive force, and that these fibrils are akin to actomyosin.10. Possible ways in which fibrillar P‐protein might be organized in the sieve elements to produce translocation are discussed. The force generated by Nitella‐type filaments at the density of P‐protein in phloem exudate would be more than adequate for the observed rates of flow. Alternatively the fibrillar arrangement in the slime mould is capable of producing volume flows as large as those in phloem. This hypothesis provides a function for P‐protein, and is also consistent with the curious ionic concentrations characteristic of sieve elements.11. It is suggested that the control by the source/sink relations of the pattern, rate and direction of flow in the phloem might be achieved by the orientation of force‐generating microfilaments by a Münch‐type flow. Such a flow is inevitable if sucrose is pumped in at one end of the path and removed at the other; it seems to be inadequate to explain the rates of mass transfer, but it might be responsible for inducing the correct orientation and polarity in the motive force.