Long Distance Transport

Plant Physiol. (1974) 54, 472-479

Long Distance TransportReceived for publication May 6, 1974

MARTIN H. ZIMMERMANNHar vard For-est, Harvard University, Petersham, Massachlusetts 01366

A few years ago, I attended a 1-day symposium on long dis-tance transport at a national meeting in a country abroad. To-wards the end of the day, as the participants became tired andno general agreement was in sight, one observer from an allieddiscipline remarked, "Why can't you translocation workersmake any progress, you still discuss the same miserable oldmodels that were proposed 40 years ago." The basis of this ac-cusation is the problem that translocation discussions are oftenpreoccupied with mechanisms about which uncertainty still ex-ists. This tends to obscure the real progress that has been made.Meetings are usually not held to review established facts, butrather to discuss unsolved problems. This symposium is an ex-ception. For once, we can lean back in our chairs and ask our-selves what was known when our society was founded in 1924,and then we can let the progress of the past 50 years parade be-fore our minds and see how much better informed we are to-day. A review of such an enormous field must necessarily be se-lective and it is rather natural that it will be a personal view.

THE TIME BEFORE 1924

This is certainly not the place for the presentation of acomprehensive history of translocation research, but a fewhighlights may set the stage before we concentrate on theperiod of the past 50 years. Older papers not specifically citedhere may be found in the bibliography of Munch's book (35).The founder of translocation research in plants was probablyMalpighi who followed up Harvey's discovery of blood circula-tion with an investigation of plants in the latter part of the 17thcentury. Stephen Hales, whose "Vegetable Statics" appearedin 1727, continued this work; he was concerned primarily withthe ascent of sap. He recognized the phenomena of root pres-sure and of transpirational pull. Phloem transport was probablydiscovered at the beginning of the 18th century by Magnol anda great deal of experimental work was done by Duhamel duMonceau later in the century, but its real significance remainedunclear until CO2 assimilation was discovered by de Saussurein 1804. A great deal of experimental work was done byKnight, Cotta, and de Candolle who began to recognize thesignificance of carbohydrate movement from the photosynthe-sizing leaves down along the stem and its storage in the form ofstarch. A related discovery of the same period was that ofdiffusion and osmosis by Dutrochet, quantified later in thecentury by the pioneering work of Pfeffer.

Translocation research reached a peak during the mid-19thcentury with the work of Hartig and Hanstein. Hartig dis-covered the sieve tube in 1837, identified exudation from bothphloem and xylem in 1860, and gave a full description of sapcirculation in xylem and phloem and of the significance of stor-age material in the stem for the following year's growth. Hesummarized his life's work shortly before his death in a bookwhich appeared in 1878 (23). Hanstein is known for his de-scription of plant polarity and, thus, of growth regulation. Hediscovered a phenomenon which even today is not fully recog-

nized by many workers, viz. that the shoot requires very spe-cific root assimilates without which it cannot develop; it doesnot merely receive water and mineral nutrients from the roots.The 19th century produced innumerable theories of sap

ascent. The "climbing theory," which originated with Malpighiand was advocated as late as 1910 by LeClerc, visualized thewater as moving up the xylem in steps and being held in placeby the ridges of the vessels in a valvelike manner. Another ob-scure concept is that of the "Jamin's chains," chains of bubblesin vessels that were said to somehow propel the water up thestem into the leaves while in fact they were a mere artifact ofpreparation. There were many others. The main problem wasthe difficulty of seeing water in the conducting elements. Waterin vessels is usually under tension, and when a preparation ismade for observation, air is drawn into the vessels. This gaverise to the notion that vessels are not normally water filled, anopinion held by the well known plant physiologist, Sachs, andmaintained by some workers until quite recently on the basisof sophisticated reasoning. Sachs also maintained that diffusionis the mechanism by which photosynthetic products are dis-tributed throughout the plant. Because of his great influence,Sachs' effect upon translocation research was rather negative,although he was undoubtedly an outstanding scientist in otherrespects.The turn of the century brought significant progress. It was

recognized that the ascent of sap in the xylem is a physicalphenomenon and does not depend on living cells (42), althoughthis concept was challenged repeatedly until relatively recenttimes. A significant discovery was the observation that twigs(4) and models involving evaporation of water from clay cups(1, 14) could raise water above barometric height. These ex-periments gradually gave rise to Dixon's cohesion theory (11).Dixon was a sort of radical among many respected scholarswho still maintained a variety of "vital" theories, including theidea that root pressure provides the necessary force to pushwater into the top of trees. However, evidence in support ofthe cohesion theory accumulated gradually. Friedrich (18), whoin 1897 invented the dendrograph to record tree growth, founddiurnal shrinkage of trees which obviously was not a result ofgrowth but of a fluctuating water content of the stem. This waslater followed up in more detail by MacDougal et al. (30).Renner was able to demonstrate tensile water in fern sporangia(37) and Dixon made the first attempt to measure tensions inplants directly (1 1).

During the first quarter of the 20th century little progresswas made in phloem-transport research. It is very likely thatinterest which had been so keen during the second part of thepreceding century turned to other problems. Plant physiologybegan to direct its attention from whole plants to specificproblems which could be investigated under controlled environ-mental conditions. Cytology, genetics, and other fields de-veloped vigorously and attracted the attention of many youngtalents. But a few efforts should perhaps be mentioned. In 1909Schneider-Orelli (38). an entomologist, published a paper on

472

LONG DISTANCE TRANSPORT

the mining moth Lyonetia clercella and reported an interesting

observation. This moth lays its eggs into the tissue of apple

leaves. The larvae hatch and eat their way through the leaf

tissue in irregular tunnels until they finally undergo meta-

morphosis, emerge from the leaf surface, and fly away.

Schneider-Orelli found that whenever the larvae had crossed

the phloem of a vein, the transitory starch in the distal leaf

area behind the injury was not exported during the night. Thus

he gave an elegant demonstration that it is the phloem through

which export of photosynthate takes place.

Dixon, the originator of the cohesion theory also did experi-

ments with phloem. He and Ball (12) initiated the measurement

of dry weight transfer into storage organs, an experimental

procedure which we shall discuss later. He was undoubtedly

much ahead of his time, and if he had the equipment available

which we have today, would certainly have made a great deal

more progress. His papers are still interesting to read and some

modern work directly continues his early attempts.

Let us now briefly consider the situation of 1924. The two

long distance transport systems, the xylem and the phloem,

were known. The xylem was recognized as carrying water and

mineral nutrients from roots to leaves. Hanstein, during the

preceding century, had gone a step further by saying that

xylem sap contains real root assimilates, but not much atten-

tion was paid to this. The cohesion theory had been proposed

by Dixon as a mechanism of sap ascent, a theory which

sounded very plausible in some ways, but incredible in others.

Water in the xylem at the tops of trees would have to be con-

tinuously under tension, i.e. in a metastable condition. There

was no satisfactory demonstration of this condition, and there

was certainly no evidence of hydrostatic gradients in trees, nor

were xylem vessels universally accepted as conduits.

Carbohydrates were known to be exported from leaves via

phloem. Circumstantial evidence suggested that the sieve tubes

were the channels of transport. Exudation from sieve tubes

appeared to indicate mass flow of a sugar solution of a concen-

tration of 10 to 30% (w/v). But there was little other evidence,

and the possibility of upward movement of root assimilates

in the bark was also discussed. This upward movement which

was supposedly taking place simultaneously with downward

movement, implied bidirectional transport in the phloem and

would preclude mass flow. But interest in phloem transport

which had slackened in the first quarter of the 20th century,

was soon to pick up.

1924-1974

In reviewing the work of the past 50 years, it is probably use-

ful if we do not look at it in a strictly chronological order, but

consider different aspects of translocation separately. Let us

first discuss the concepts of the mechanism of xylem transport.

Mechanism of Sap Ascent. The cohesion theory had already

been formulated, but its feasibility was under debate. The

concept is so utterly simple that it was criticized immediately.

Proponents of vital theories produced evidence which seemed

to preclude a purely physical phenomenon. Many reports con-

cerned a failure of sap ascent at slightly above 0 C. Leaves on

branches of trees were reported to wilt when the basal part of

the branch was surrounded with ice. Under more controlled

conditions, reversible wilting of tree saplings was even reported

as long as the stem was held at 2 C (22). Repetitions of these

experiments finally indicated that the results had been a result

of instrumental deficiencies (53). Another fundamental prob-

lem was that many of the experimental procedures that were

used to kill stem tissue destroyed the physical integrity of the

xylem-transport system. Heating or freezing the xylem intro-

duces bubbles and thus causes embolism. Drying of the xylem

produces cracks and renders the water-conducting channelsleaky.To some investigators the cohesion theory appeared incredi-

ble, because it postulates that water in the xylem at the top oftrees is under tension at all times. This is difficult to believewhen one considers that tensile water is metastable and thattrees are quite frequently tossed about in the wind. Researchproceeded along several lines simultaneously. There was thequestion of how much tension a water column can withstand.Many papers dealt with this question and although the answersdo not all agree, it seems that in the majority of cases the re-ported tensile strength of water was sufficiently high to makethe cohesion theory feasible. But the crucial question, whetherwater in the xylem of plants is under tension, and whether, in atall tree, these tensions line up along the stem to form a hydro-static gradient, remained until the 1960's, although measure-ments of leaf-water potentials at different heights in trees hadpointed earlier in the right direction. It was not until Scho-lander et al. (39) introduced his "pressure bomb" that tensiongradients in trees could be measured more or less directly.Interestingly enough, Scholander had been one of the critics ofthe cohesion theory who repeatedly pointed to the lack of di-rect evidence. Another interesting fact is that early attempts tomeasure negative pressures in plant tissues by counterbalancingthem with a positive pressure had been made by Dixon, butunfortunately his attempts were stalled by technical difficulties(11). Today psychometric and piezoelectric devices are alsoused to measure tension gradients in trees, but like the earlierleaf-water-potential measurements, these methods are moreindirect and do not show tensions in the xylem as directly asthe pressure bomb.

Structural Aspects. Xylem structure has been well knownfor over100 years, and surely nobody expected any excitingnew discoveries in this field. Yet, it was largely the lack ofappreciation of structural aspects that, for many years, hadbeen a stumbling block in the understanding of sap-ascentproblems. Xylem water is confined to millions of self-containedcompartments which form a very complex network. Passageof water from one to the next takes place through pits alonglengths of vessels wherever they run in pairs. The interestingthing is that these parallel runs are sufficiently long that passageof water from one to the next does not represent excessiveresistance to flow. Yet the pit pores are so small that they donot permit an air-water interface to penetrate (56). This ar-rangement enables the plant to conduct the water efficientlywithout excessive loss of safety. Among trees, we find conifersand small porous species operating at a high safety and rela-tively low efficiency level, and large porous species operatingat very high efficiency but at greater risk. Both strategies aresuccessful in their own right, but high efficiency requires theproduction of new xylem every spring before the leaves emerge(56). The high risk strategy occasionally hastens the downfallof a species as we have witnessed in the case of the blight ofthe American chestnut since the beginning of this century andalso of the Dutch elm disease which is wiping out elms today.Much of the uncertainty about the cohesion theory of sap

ascent is put to rest if we think in terms of three-dimensionalwood structure. Plants contain a very great number of smallconducting units and failure of a few may cause only smalldamage. Sap flows around double sawcuts because of the lim-ited length of some of the vessels and because of their complexnetwork which enables the water to flow around injuries onalternate paths.The Beginning of Quantification. It was another important

move during the past 50 years. Not only parameters crucial interms of mechanism, such as tensile strength of water, pres-sures, gradients, and others were measured, but also quantities

473Plant Physiol. Vol. 54,1974

Plant Physiol. Vol. 54, 1974

of interest in themselves. In 1938 Huber and Schmidt (25, 26)introduced their heat-pulse method to measure sap velocities.The reliability of this method in absolute quantitative terms isstiil being debated (24). But, the method yielded immediately a

number of important comparative results. For the first time itwas possible to monitor sap velocity in tree stems during a24-hr period and throughout the year. Velocities within a singletree showed that, depending on species, sap movement speedsup or slows down from base to apex. When diurnal sap veloci-ties in the top of the stem were plotted against those at thebase, an interesting hysteresis curve resulted, showing that sapmovement is initiated in the morning from the top of the tree,i.e. by transpiration from the leaves. These curves agree withthe concept of elasticity of the tree trunk. Indeed, dendro-graphic measurements at two heights show that the stemshrinks first in the upper and later in the lower part whentranspiration begins in the morning (25).

Another interesting finding was that sap velocities correlatewith vessel or tracheid size. In other words, sap velocities inwide porous trees are very much larger than those of narrowporous trees and the energy dissipation by water transport inspecies with different vessel sizes is quite comparable.

Quantification has proceeded in many other fields. Aninteresting application of irreversible thermodynamics byTyree and Zimmermann (48) opened up the possibility of mea-suring volume flow electrically. The Onsager equations showhow sap flow in the stem is related to electric flow. Althoughthe latter is very small, it is possible to use it to measure volumeflow. Although Tyree's delta-I technique is still troubled bycalibration difficulties, once it is perfected for practical use,it will be of invaluable help to plant ecologists.

The Difference Between Trees and Herbs. Although weknow that herbs and trees are diuerent, all too often we liketo generalize and, when talking about trees, use concepts thathave been found or verified in herbs, or vice versa. Recentyears have made us very cautious, because they have broughtsome very surprising findings. Passioura (36) reported sapvelocities in the xylem of wheat under drought conditions of2900 m/hr. This is very much larger than the fastest veloci-ties of large porous trees (25). At the same time pressuregradients must be correspondingly very much steeper than anyknown in trees. Because herbs do not have to cope with height,they can be extravagant with their pressure gradients.

Another series of reports, equally shocking to someonefamiliar with the "normal" situation as we know it from trees,are those of Milburn and McLaughlin (33) who found thatvessels of herbs may regularly embolize during the course of ahot summer day. The damage is repaired during the night byroot pressure. Embolism can be heard with sensitive listeningdevices as a series of clicks, presumably one per embolizingvessel.The Extrafascicular Path of Water. The concept of the apo-

plast or free space, continuous with the xylem, whose water po-tential is in equilibrium with that of the living cells, enables usto understand the irrigation of the plant as a whole and ex-plains the relatively rapid spread of water to all cells. I cannotgive a comparative figure of water volume in the large conduct-ing spaces (tracheids and vessels) versus that of walls and cellvolumes, but the water "storage" area, i.e. the water volumeoutside the long distance conducting space, must be considera-ble. We know that the diurnal shrinkage of tree stems is at leastpartly a result of volume decrease of tissues other thantracheids and vessels. Water movement outside xylem takesplace through cell walls as Strugger has so elegantly demon-strated with his fluorescent dye experiments (43). Hydraulicconductivity in certain cell walls may be low (50). but distances

to the xylem ends in the roots and from the xylem ends to thestomata are very short.

Solute Transport in the Xylem. Not only water, but alsomineral nutrients ascend from roots to leaves in the xylem.Although this was known in 1924, textbooks usually visualizedthis a bit too naively. Hanstein (35) had recognized in the lastcentury that the shoot depended on roots as organs of metabo-lism and not only as ports of entry for mineral nutrients. Thisconcept of roots as "secretory organs" gained ground onlyrather slowly, but it is quite acceptable today (28). Many of thesolutes of xylem sap are in organic form and contain vitalgrowth factors such as cytokinins without which the shoot isunable to develop. Certain ions such as iron must be broughtinto a chelated form so that they can move (5).Phloem Transport in the Past 50 Years. A review of con-

cepts in phloem transport is more difficult to write, becausethis field is now in a much greater state of flux and there aremore uncertainties than in xylem transport. These uncertain-ties concern primarily the mechanism of transport and it is per-haps better to de-emphasize mechanisms and concentrate moreon aspects in which real progress has been made. Phloem-trans-port research has seen considerable development in methods.We can now do things that were unheard of 50 years ago. Letus very briefly consider the major methodological advances.Substances that are translocated in small quantities can beanalyzed now with relative ease; we know much better what itis that moves. The availability of radioactively labeled sub-stances in combination with chromatographic methods andmodern instrumentation for measuring radioactivity has per-mitted a sophistication of analysis unheard of in the 1920's.The aphid stylet technique (27) permits us to sample singlesieve elements. Electron microscopy gives us a very close lookat structural aspects of phloem. Let us now look at some ofthese aspects in more detail.

Localization of Transport. The recognition of phloem as thetissue responsible for export of photosynthetic products fromleaves has been described before. The observation of the ac-tivity of leaf-mining larvae had been almost an accident, but itis a beautiful example of keen observation. Work in the 1920'sand 1930's was more directed. Schumacher (40) isolated thephloem strand of the central conducting bundle of the petioleof Pelargoniiumii by surgical means and showed again thatphloem is the site of export from the leaf. Mason and Mlaskell(31) in a long series of papers on transport in cotton found thatthe site of sugar transport is the inner bark of the stem and thatthe main transport substance is probably sucrose.

Based on Hartig's observation of phloem exudation, Dixonand Gibbon (13) forced a dilute solution of potassium ferro-cyanide into the phloem and was able to show afterwards, bvmeans of ferric choride. that movement had taken place in theinnermost phloem layer of the bark. A similar method wasused by Tammes (45) to show that exudation from tapped palminflorescence stalks is of phloem origin. Dixon also experi-mented with pressure injection of India ink, a method whichhas been perfected so elegantly by Barclay and Fensom (2)during recent years.The most widely used method for the localization of trans-

port was, of course, tissue autoradiography after transport ofradioactively labeled photosynthate. Earlier findings were con-firmed and by gradual refinement it was shown that transporttakes place, as had been suspected all along, in the sieve tubes(46).

Beginning with the 1950's it became possible to tap individ-ual sieve tubes by letting aphids feed on phloem, cutting themfrom their mouth parts, and collecting the exudate flowingfrom the cut stump of the stylets (27).

474 ZIMMERMANN


Nature of Translocated Substances. Analyses of sieve tubeexudate from incisions and from aphid stylet bundles enabledus to find the form in which organic substances are translo-cated. Sucrose is probably the most important transport sugar,but other forms like the raffinose family of oligosaccharidesand sugar alcohols are prominent in certain plant families (56).This finding was confirmed with tracer studies. It seems to bequite simple and logical to let the plant photosynthesize with"4CO2 and then to extract the stem to see what substances arefound in transit. But this procedure is subject to erroneous con-clusions because it is not immediately obvious which of theextracted radioactive substances are actually translocates andwhich are secondary stationary products. The problem wasovercome in two ways. A time-distance study in the grape re-

vealed that the ratio of sucrose/hexose increases with translo-cation distance. This indicates that sucrose is the moving sub-stance, hexose the secondary stationary product (44). In otherexperiments, double grafts of sunflower and Jerusalem arti-choke were used. These plants have different storage sugars. Inthis way it was again possible to distinguish sucrose, the movingsugar, from storage products (29). A whole array of substancesis now known to be mobile (52).

Phloem Structure. To write about structural concepts is per-haps the most difficult task. Surely, considerable progress hasbeen made in phloem anatomy, but seeing more detail does notnecessarily result in conceptual progress. I do not mean this inany negative way, because electron microscopy has resultedcertainly in a great deal of new knowledge. Early electronmicrographs showed that the sieve pores were plugged andmade one wonder how translocate would ever get through.Fixation procedures improved rapidly, and present day elec-tron micrographs show pores to be more open than those ofonly a few years ago. Conceptual results of electron microscopyof phloem have been mostly speculative and concern deduc-tions about possible mechanisms of transport. These deduc-tions, when derived from other additional evidence such aslight microscopy of isolated phloem strands, may prove to bevery useful in the long run, but I believe it is safe to say thatthey still must be regarded as very tentative.

Doubtless, the most important structural concept is that ofthe sieve tubes' sealing mechanisms. While, in the xylem ves-sels, transverse walls have disappeared completely during evo-lution in the most advanced species, the plant could not affordthis with their sieve tubes. The explanation is a very simple one.Since xylem pressures are below atmospheric most of the time,any injury fills the severed vessel with air, sealing it auto-matically from any neighboring vessel. Sieve tubes, in contrast,are under high positive pressures, and any injury causes a lossof photosynthate. If there were no sieve plates, the loss wouldbe continuous along the whole sieve tube and would even in-volve mobilization of reserves along the way. Sieve platesprovide sites at which transport is stopped in case of injury.Thus the maintenance of plates during evolution was a distinctadvantage. There are at least two sealing mechanisms, both ofwhich function quite rapidly. P-protein surges toward an injurywhen turgor is released and plugs the pores which are subse-quently closed by more permanent callose seals (15).

Quantifying Phloem Transport. Among the most importantadvances of the past 50 years has been the beginning ofquantification of phloem transport. Quantification concernsfacts and figures, and it is interesting to see that many of thefactual results were sought to test specific concepts. Perhapsone of the best examples is the observation and measurementof mass transfer, movement of dry weight within a given unitof time. If this is expressed per transverse-sectional areathrough which movement has taken place, we speak about

specific mass transfer (SMT), which can also be expressed as a

flowing solution.

Specific mass transfer (SMT8t) = concentration X velocity(g hr-'cm-2) = (g cm-3) X (cm hr-')

If we assume that the sieve tubes are the translocation chan-nels, we have to express mass transfer per transverse-sectionalarea of sieve tubes. This is what the subscript in the termSMTSt indicated. It is sometimes not easy to recognize sievetubes in transverse sections. For convenience, therefore, masstransfer is often expressed per total phloem (SMTph), with theimplication, of course, that the value cannot be used directlyin the above equation, because the velocity value on the rightside of the equation would not be very meaningful. Most in-vestigators use an earlier estimate that sieve tubes constituteabout 20% of the phloem's transverse-sectional area. Newermeasurements showed this figure to be somewhat low, more-over it is quite variable from species to species (6).

It is rather interesting that specific mass transfer at peakperformance is a rather well defined figure, regardless of plantspecies. For dictoyledonous stems, expressed per whole phloem,it is between 3 and 5 g cm2 hr-'. This has been measured manytimes by recording the dry weight increase of potatoes, fruits,and others (6). If it were expressed per transverse-sectional areaof sieve tubes we would have to multiply this figure by a factorof two to five, depending on what percentage the sieve tubescomprise.The concept of velocity on the right side of the equation

merits special attention. As it stands it implies a moving liquidcylinder. This does not exist in nature. Even the simplest case,Poiseuille flow through long capillaries such as we find in thexylem of large porous trees, is not cylindrical, but paraboloidal,with velocities ranging from zero at the capillary wall to apeak velocity at the center equal to twice the cylindrical value(Fig. 1). This is so because the volume of a paraboloid is equalto the volume of a cylinder of equal diameter and half theheight. The important question now arises of how do we mea-sure experimentally the cylindrical velocity needed on the rightside of the equation. This will have to be done with great care,especially if velocities are graded. There are two possibilities.One is to try and find in the literature a case where velocitiesare quite uniform. This appears to be the case in the sugar beetpetiole, where the rate of the advancing front is more or lesslinear and does not become appreciably flatter with time. Inone of Mortimer's (34) reports, the advancing radioactivityfront indicates a fairly uniform velocity of about 50 cm/hr.Another type of measurement, that of an advancing concentra-tion ratio wave in a tree, also gives a cylindrical value ranging,in this case, from 30 to 70 cm/hr (54).

If we assume that sieve tube exudate is a representativesample of a solution flowing through the sieve tubes, we wouldhave to multiply the cylindrical velocity with the exudate con-centration and thus would obtain an SMTs, value. Sieve tubeexudate usually is of a concentration of 0.1 to 0.2 g cm-9andwhen it is multiplied with 50 cm hr-', we arrive at an SMT.t of10 to 20 g cm-2hr-', a value which corresponds quite closely tothe SMT values found as increases of dry weight. In otherwords, it is not unreasonable to assume that transport takesplace in the form of a flowing solution.The concept of velocity is quite confused in the literature.

Most advancing radioactivity fronts are not as simple as theone cited above and it is worthwhile to give them more carefulthought. Let us again take first a simple case, that of capillaryflow. If we take an advancing flow paraboloid and plot itsprogress in the form of advancing profiles, we arrive at a series

Plant Physiol. Vol. 54, 1974 475


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FIG. 1. Top: Poiseuille flow in a capillary of the radius r. Mole-cules behind the origin at time to advance as a paraboloid whichlengthens with time (t, and t2). Center: Moving volumes or labeledsolutes plotted at t, and t2 show a linear slope that becomes flatterwith time. The peak velocity of paraboloidal flow in the capillarycenter can be read from the advancing profile as the longest distancetraveled during a given time (e.g. 8 distance units during the timet-to). Bottom: The mass transfer equation uses the concept of amoving liquid cylinder, i.e. all molecules are assumed to move atequal velocity. The same volume, shown above as a paraboloid, isshown here moving as a cylinder. The "cylindrical" velocity is thedistance traveled by the advancing vertical profile per unit time. It ismarked by the arrow (cv) and equals four distance units during thetime t1 - to. The center diagram shows how to read the cylindricalvelocity from the advancing front of paraboloidal flow. Note thatthe cylindrical velocity is exactly half the peak velocity of parabo-loidal flow, because a cylinder of equal diameter and equal volumeis half as long as a paraboloid.

of straight lines whose slope decreases with time, all turningaround a single point, the maximum capacity of the capillary,at the origin (Fig. 1, center). The peak velocity is then thefastest moving component and the cylindrical velocity is theadvancing point of half the final concentration.'

So far we have assumed that we measure only moving ma-terial. In fact, in most plants a good portion of the radioactivityis unloaded in transit and stays behind. What we then measureis an advancing front of moving and stationary material. Thisdoes not give linear profiles, but rather profiles in which radio-activity decreases logarithmically from the origin (49, 51). Inother words, of the moving material only a certain percentagemoves on and the rest stays behind (Fig. 2). It is quite obvious

'Note Added in Proof. It has been calculated and proved ex-perimentally that, depending on capillary diameter, flow velocity,etc., radial diffusion may become so significant that solute appearsto move nearly cylindrical with little grading of velocities, in spiteof paraboloid flow. (Taylor, G. 1953. Dispersion of soluble matterflowing slowly through a tube. Proc. Royal Soc. London A219:186-203).

that when two different substances move simultaneously at thesame velocity and their unloading rates along the path are notthe same, different translocation velocities can be measured(Fig. 3). Figures 2 and 3 represent very simplified models;readers will find more detailed discussions of profiles in theliterature (e.g. 51).

Let us now look at other aspects of translocation research inwhich quantification is making progress. One of them is phloemloading, i.e. the secretion of sugars into the sieve tubes againsta concentration gradient. This seems to take place stepwise,from phloem parenchyma to companion cells and sieve tubesbut the pathway is not yet entirely clear (20). Still anotheraspect is the quantitative measurement of translocation alonga pathway, part of which is subjected to anaerobic conditionsor to metabolic poisons. The nature of this inhibition might beloss of semipermeability, sieve pore plugging, or still anothercause (19). The crucial question is whether or not metabolismalong the path is involved in the translocation process directlyor merely indirectly, by maintaining the integrity of the chan-nel (19).

Still another quantification effort concerns pressures. Ifphloem transport is a pressure-mediated mass flow, one shouldfind turgor gradients from sources to sinks. So far, most evi-dence is quite indirect and we are only just beginning to beable to get direct measurements (21). Measurements of sievetube conductivities are also still in their infancy, but effortsare under way and will undoubtedly assume more importance.Numerous persons have used the extensive quantitative in-

formation in the literature to produce mathematical models

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FIG. 2. The dashed lines indicate the advancing profile of a la-beled solute at even (cylindrical) velocity. If 20% of the solute isunloaded at each unit of distance, the moving solute is representedby the profile marked M. If this procedure is carried out over 10distance units during the time to to t,, the profile A results, represent-ing moving and stationary solutes. If the procedure is carried outover 20 distance units in 20 steps, during the time to to t2, the profileB results.

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ZIMMERMANN476


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FIG. 3. Profiles like A and B in Figure 2 plotted on a logarithmicscale (with the distance retained linear) result in nearly straightlines. If this is done for two different unloading percentages (e.g. fortwo different solute species), the profiles simulate different veloci-ties. Theoretically the two solute species reach the same distancewithin a given time, but this may not be detectable because a sub-stance can only be detected above a certain threshold concentration,here arbitrarily set at concentration one (the abscissa).

of the translocation process in order to see which of thetheories of proposed mechanisms fits it best (17). One of theproblems here is the fact that nature is very complex and thatmodels are always based on certain simplified assumptions.Nevertheless, results have been interesting and will probablyincrease in importance as models become more sophisticated.The Mechanism of Phloem Transport. With this topic we

are getting to the very heart of transport concepts. In contrastto sap ascent in the xylem we have not yet reached generalagreement and this area is the center of controversy today. Thesearch for an explanation of the transport phenomenon, in fact,has stimulated most of the efforts during the past 50 years.

Let us begin with the direction of transport. It is recognizedquite generally that phloem transport is continuous fromsources to sinks, i.e. from points of production to points ofconsumption. In very broad terms this is from the green leavesto places of growth and storage, and, at times of mobilization,from places of storage to places of growth (8). The direction oftransport is therefore generally, e.g. in a tree, basipetal (down-ward). It is acropetal in certain special cases, such as in grow-

ing shoot tips, flowers, and fruits. Up to this point everyone isin agreement. But as soon as we go a step further, the difficultybegins. We can ask whether all substances move in the same

direction at any one time and through any one channel, or ifeach substance moves individually from its source to its sink.This question is usually formulated in a different way; do nutri-ents move through the sieve tubes in the form of a solution, or

do they move independently of solvent water? Superficially thisproblem appears to be easy to solve, but, in fact it is not. Thepoint is that the plant is so well organized and carries out itsfunctions so efficiently that experiments become ambiguousvery easily. Let us take the relatively simple question ofwhether certain root assimilates move upwards in the bark.This question has been investigated repeatedly during the pe-

riod of the past 50 years. Proponents of the mass flow concept

say that movement in the phloem of the lower part of a plant

stem is downward under normal conditions, sugars and perhapsa few other substances moving into the roots. Nutrients synthe-sized in or absorbed by the roots ascend in the xylem. Othersmaintain that certain substances move up from the rootsthrough the bark while at the same time sugar movement isdownward. What is the evidence? The problem looks verysimple. One can "girdle" a stem (remove a ring of bark) and seewhether the shoot still receives sufficient root nutrients. It doesnot, and there is a distinct decrease in root-nutrient supply. Isthis because we have interrupted the channel for the ascent ofroot nutrients? Or is it because we have starved the roots andthus prevented them from fulfilling their function properly?The answer is ambiguous. When radioactive tracers becameavailable, the following experiment was conceived and repeatedmany times to solve the problem. Over a length of stem, barkwas separated from wood with a piece of wax paper. One iso-tope, e.g. 14C, was applied to a leaf above, another, e.g. 32P, toa leaf below the stem section where xylem and phloem wereseparated. After a certain time had elapsed, usually a fewhours, the isolated bark strip was analyzed. Both tracers weredetected. This was taken as evidence that one of the tracers hadmoved into it from above, the other from below. But did theydo this? Visualize translocation velocities, several m/hr inthe xylem and perhaps 1 m/hr in the phloem. How many timescould these substances have circulated within the plant duringthe experimental time and moved into the bark strip togetherfrom above?A newer version of the experiment employs aphids or aphid

stylets. An aphid colony draws nutrients from both sides be-cause it is a strong sink. But, at the same time, transport cango on in the normal direction through unpunctured sieve tubes.An aphid colony can draw tracer into an old leaf from a pointof application elsewhere in the plant, whereas, through un-punctured sieve tubes, normal export from the leaf takes place.But this is not bidirectional transport in the controversial sense.Some pretty hard evidence for bidirectional transport througha single sieve tube has been produced by Trip and Gorham(47), although even their data are not unequivocal. The validityof experimental evidence is rarely absolute; it always dependson more or less subjective interpretation.A final statement concerning bidirectional transport should

be made. So far we have been concerned with the concept ofsimultaneous bidirectional movement in a single conduit whichwould not be possible in the form of a flowing solution. If welook at a growing shoot tip, we always find bidirectional trans-port in the stem section between newly matured leaves, becausethese always transport in both an acropetal and a basipetal di-rection. The vascular anatomy in this area is so complex thattransport in different directions can be maintained easily indifferent channels (3).One of the fundamental questions is whether phloem trans-

port takes place in the form of a flowing solution. It is indeedvery difficult not to believe in a flowing solution when onecan observe, for hours or days, exudation from a severed aphidstylet bundle at a rate requiring continuous refilling of the sieveelement three to 10 times per sec. (56). The question ariseswhether this mass flow is pressure actuated and pressure regu-lated. This proposal was made by Munch in 1926 and wasoutlined in more detail in his book in 1930 (35). In theopinion of many investigators this is still by far the best expla-nation (8). One of the satisfying aspects of this mechanism isthat it would be completely self regulating and, in conjunctionwith the xylem movement, would enable the plant to move anysubstance practically to any point within the plant body (8, 32).

Another mass-flow theory is Spanner's (41) proposal ofelectro-osmotic flow, which is supposed to be driven by a

477Plant Physiol. Vol. 54, 1974


metabolic maintenance of an electric potential across the sieveplates. In this case, pressure would be merely the signal for theregulation of flow. Visualize e.g., two incisions very close to-gether, both interrupting the same phloem strands of a treestem. Flow towards the upper incision is downward, flowtowards the lower from below. Munch's pressure-flow theorysimply requires flow towards the point of lowest pressure, i.e.the incisions. Spanner's theory would require an instantaneouselectrical polarity reversal in the phloem below the incision,perhaps pressure triggered.

There are many other proposals such as maintenance oftransport by pulsations of microstructures in the sieve tubes or

protoplasmic streaming, a proposal first made by de Vries in1885 (10), and re-emphasized by Curtis (9) and others duringmore recent times (7). Protoplasmic streaming has not beenreported reliably in sieve tubes, nor has any proposal ade-quately explained the magnitude of mass transfer.

There are many other proposals, for which I refer you tothe literature for a more detailed description (16). In addition,there are quite a number of investigators who do not believe inany of the proposed mechanisms and merely regard the prob-lem as unsolved. It is of course possible, and perhaps even

likely, that transport through the phloem is driven by morethan a single mechanism. If this is the case, experimental evi-dence is even more difficult to assess than if we were dealingwith only one mechanism. So, let me conclude my descriptionsof concepts of translocation mechanisms even though it is onlya fragmentary one.

A LOOK INTO THE FUTURE

Where are we going from here? Surely, I am not a prophetto tell you what will happen during the next 50 years, but it isstill fascinating to speculate in what direction we might begoing.From an evolutionary point of view, plants have often found

different ways of solving the same problem. In sap ascent,height of a tree, drought of the soil, or salt-water environmentof the roots of a mangrove tree are all physiological hurdles toovercome. Special environmental conditions have often broughtabout special solutions. It was a surprise to learn that there areherbs that can afford to let the vessels embolize during the day,because they can refill them at night (33). Others appear tomove water extremely fast along an incredible steep pressuregradient; they can do so because they are very short (36).Further surprises may come from the study of aquatic angio-sperms. Roots, often regarded here as mere holdfasts, mayrepresents secretory organs that pump small amounts of spe-cific nutrients to the leaves which depend on this method ofnutrition. Xylem of submerged plants can be very different instructure because the xylem sap is not under tension. Rigidxylem cell walls are not needed. Furthermore, the sealing sys-tem we are familiar with in xylem does not work if apoplasticsap is under positive pressure. The structural requirements ofan aquatic plant are therefore quite different. The Casparianstrip is more important, or a tight epidermis or periderm mustprotect the plant from root-nutrient loss or both. Evolutionaryadvantges lie not only in a development of efficiency, but alsoin a maintenance of safety. Other structural features, crucialfor the proper functioning of the translocation system, willhave to be recognized.

It has been accepted almost as dogma that sieve tubes func-tion only for a very short period i.e. that they work with a sortof built-in functional absolescence. Do they really? There arearborescent monocotyledons like palms in which sieve tubes,once formed, may have to remain functional for 100 years ormore.

Many detailed questions await resolution. The function ofthe apoplast in cell to cell movement in leaves and roots is stillnot satisfactorily resolved. Perhaps one of the most importantand fascinating problems is that of regulation of phloem trans-port. Visualize a palm of the habit of Corypha which storesstarch in its stem throughout the course of its whole life, per-haps 50 years, and then produces a terminal inflorescence andmoves 600 kg of carbohydrates into the fruits within a singleyear (55). The pressure-flow theory could explain how theinflorescence signals the stem to mobilize its reserves. But isthis the correct explanation?Much of the information we have must be further quanti-

fied. The question of mechanism of phloem transport is notyet resolved, at least not to everybody's satisfaction. Is thereonly one mechanism or are more than one operating? If so.how important are the individual components from a quantita-tive point of view? We could go on and on asking questions.Most of the answers will perhaps be reviewed in another 50years when our Society will hold its centenary symposium.1. ASEENASY, E. 1893. Ueher das Saftsteigen. Vebl. nattir-wiss.-med. Ver. Ileilllb.,

Vol. 5. (Ref. in Bot. Cbl. 62 :237-238).2 BARCLAY, G. F. AN-D D. S. FENSOMi. 1973. Passage of carbon black tlhroulglh sieve

plates of unexcised Heraclewn, sphonzdyliumiii after microinjection. Acta Bot.Neer. 22: 228-232.

3. BIDDULPH, 0. AND R. CORY. 1960. Demonstration of tw-o translocation mechla-nisms in studies of bidirectional movement. Plant Physiol. 35: 689-695.

4. BbHMI, J. 1893. Capillaritit und Saftsteigen. Ber. Deut. Bot. Ges. 11: 203-212.5. BOLLARD, E. G. 1960. Transport in the xylem. Anno. Rev. Plant Physiol. 11:

141-166.6. CANNY, M. J. 1973. Plhloemii Translocation. Cambridge University Press.7. CANNY, M1. J. 1973. Protoplasmic streaming. In: Al. H. Zimmermann and J.

A. Mlilburn, eds., Transport in the Phloemii. Encyclopedia of Plant Physiol-ogy (N.S.), Springer-Verlag, Heidelberg. In press.

8. CRAFTS, A. S. AND C. E. CRISP. 1971. Phloem Tiansport in Plants. W. H. Free-man and Co., San Francisco.

9. CURTIS, 0. F. 1935. The Translocation of Solutes in Plants. MIcGraw-Hill BookCo., New York.

10. DE VRIES, H. 1885. Ueber die Bedeutung der Circulation und der Rotation desProtoplasmas fuir deni Stofftransport in der Pflanze. Botanische Zeitung43: 1-6, 18-26.

11. DixoNx, H. H. 1914. Transpiration and the Ascent of Sap in Plants. MacmillanPublishing Co., Inc., London.

12. DIxoN, H. H. AND N. G. BALL. 1922. Transport of orgallic substances in plants.Nature 109: 236-237.

13. DIxoN, H. H. AND M. W. GIBBON. 1932. Bast sap in plants. Nature 130: 661.14. DIXoN, H. H. AN'D J. JOLY. 1896. On the ascent of sap. Phil. Trans. Roy. Soc.

London Ser. B 186: 563-576.15. ESCHRICH, W. 1975. Sealing systems in phloem. 1I1: M. H. Zimrmermann and

J. A. 'Milburn, eds., Transport in the Phloem. Encyclopedia of Plant Phys-iology (N.S.), Springer-Verlag, Heidelberg. In press.

16. FEN-SONM, D. S. 1975. Other mechanisms. In: M. H. Zimmermann and J. A.Milburn, eds., Transport in the Phloem. Encyclopedia of Plant Physiology

(N.S.), Springer-V erlag. Heidelberg. In press.17. FISHER. D. B. 1970. Kinetics of C-14 translocation in soybean. Plant Physiol.

45: 107-125.18. FRIEDRICH, J. 1897. Ueber den Einfluss der Witterung auf den Baumzuwachs.

Zentbl. ges. Forstw. 23: 471-495.19. GEIGER, D. R. 1975. Effect of temperature and metabolic inhibitors. In: Ml. H.

Zimmermann and J. A. Milburn, eds., Transport in the Phloem. Encvclo-pedia of Plant Physiology (N.S.), Springer-Verlag, Heidelberg. In press.

20. GEIGER, D. R., R. T. GIAQL-INTA, S. A. SOVONICK AND R. J. FELLOWS. 1973.Solute distribution in sugar beet leaves in relation to phloem loadling andtranslocation. Plant Physiol. 52: 585-589.

21. HAMMEL, H. T. 1968. Measurement of turgor pressure anid its gradient in tIlephloem of oak. Plant Physiol. 43: 1042-1048.

22. HANDLEY, W. R. C. 1939. The effect of prolonged chiilling on water movementand radial growth in trees. Ann. Bot. 3: 803-813.

23. HARTIG, T. 1878. Anatomie und Physiologie der Holzpflanzen. Springer-Verlag,Berlin.

24. HEINE, R. W. AND D. J. FARR. 1973. Comparison of lleat-pulse and radioisotopetracer methods for determining sap flow velocity in stem segments of poplar.J. Exp. Bot. 24: 649-654.

25. HUBER, B. AND E. SCHnMIDT. 1936. Weitere thermo-elektrische U-ntersucllitngenuiber den Transpirationsstrom der Biiume. Tharandt. forstl. Jb. 87: 369-412.

26. HUBER, B. AND E. SCHIMIDT. 1937. Eine Kompensationismethlode zur tllermo-elektrisclien Messung langsamer Saftstrome. Ber. Deut. Bot. Ges. 55: 514-329.

27. KENNEDY, J. S. AND T. E. MIITTLER. 1933. A metlhodl of obtaining lplIoeii sapv ia the mouth parts of apllids. Nature. 171: 328.

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