Tansley Review No. 22 What becomes of the transpiration stream?

Changes of view on the course of the transpiration stream beyond the veins in leaves are followed from the imbibition theory of Sachs, through the (symplastic) endosmotic theory of Pfeffer (which prevailed almost unquestioned until the late 1930s), to Strugger's experiments with fluorescent dye tracers and the epifluorescence microscope. This latter work persuaded many to return to the apoplastic-(wall)-path viewpoint, which, despite early and late criticisms that were never rebutted, is still widely held. Tracer experiments of the same kind are still frequently published without consideration of the evidence that they do not reveal the paths of water movement. Experiments on rehydration kinetics of leaves have not produced unequivocal evidence for either path. The detailed destinies of the solutes that reach the leaf in the transpiration stream have received little attention. Consideration of physical principles governing flow and evaporation in a transpiring leaf emphasizes that: (1) Diffusion over interveinal distances at the rates in water will account for substantial solute movement in a few minutes, even in the absence of flow. (2) Diffusion can occur also against opposing now. (3) Volume fluxes in veins are determined by the diameter of the largest leaves examined contain high conductance supply veins which are tapped into by low-conductance distributing veins. (4) Edges and teeth of leaves will be places of especially rapid evaporation, and they often have high-conductance veins leading to them. (5) Solutes in the stream will tend to accumulate at leaf margins. On the basis of recent work, the view is maintained that the water of the stream enters the symplast through cell membranes very close to tracheary elements. Also, that this occurs locally over a small area of membrane. Many solutes in the stream are left outside in the apoplast. This produces regions of high solute concentration in the apoplast and an enrichment of solutes in the stream as it perfuses the leaf. Solutes that enter the symplast are not so easily tracked. Suggestions about where some of them may go can be gained from a fluorescent probe that identifies particular cells (scavenging cells) as having H⁺ -ATPase porter systems to scrub selected solutes from the stream. Unpublished case-histories are presented which illustrate many aspects of these processes and principles. These are: (1) Maize leaf veins, where the symplastic water path starts at the parenchyma sheath; (2) Lupin veins, where the symplastic path starts at the bundle sheath and where solutes are concentrated in blind terminations; (3) The edges of maize leaves where flow is enhanced by a large vein (open to the apoplast), and solutes are deposited in the apoplast by evaporation; (4) Poplar leaf teeth, which receive strong flows, and where the epithem cells are scavenging cells; (5) Mimosa leaf marginal hairs, which have scavenging cells at their base; (6) Active hydathodes, whose epithem cells are scavenging cells; (7) Pine needle transfusion tissue, which is a site of both solute enrichment (in the tracheids), and scavenging (in the parenchyma); (8) Estimates are made of diffusion coefficients of a solute both along and at right angles to the major diffusive pathway in wheat leaves. The first is 1000 times the second, but is 1/100 of free diffusion in water. Five general themes of the behaviour and organization of the transpiration stream are induced from the facts reviewed. These are: (1) The stream is channelled into courses of graded intensities by the interplay of the physical forces with the anatomical features, each course with a distinct contribution to the processing of the stream. (2) Water enters the symplast at precise locations as close as possible to the tracheary elements. (3) As the stream moves through the leaf its solute concentration is enriched many-fold at predictable sites. (4) Solutes excluded from the symplast diffuse from these sources of high concentration in specially formed wall paths, in precise patterns, at rates which can be measured, and which are low compared with diffusion in water. (5) Other solutes permeate the symplast, often over the surfaces of groups of cells which are organized into recognized structural features. CONTENTS Summary 341 I. What becomes of the transpiration stream ? 342 II. Review 343 III. Preview 355 IV. Overview 361 Acknowledgements 365 References 365.