REVIEW ARTICLE Xylem-Phloem Exchange Via the … · REVIEW ARTICLE Xylem-Phloem Exchange Via the Rays: The Undervalued Route of Transport ... delivery from the ray into the sieve

Journal of Experimental Botany, Vol. 41, No. 227, pp. 631-644, June 1990

REVIEW ARTICLE

Xylem-Phloem Exchange Via the Rays: TheUndervalued Route of Transport

AART J. E VAN BEL

Transport Physiology Research Group, Botanical Laboratory, University of Utrecht, Lange Nieuwstraat 106, 3512 PN Utrecht, TheNetherlands

Received 18 September 1989

ABSTRACTThe radial solute exchange between xylem and phloem is an important determinant of the nutrient distnbution and C/N economyof seed plants. Nevertheless, our knowledge of the mechanism of xylem-phloem exchange is very limited. This paper aims tointegrate anatomical and physiological data about xylem-phloem exchange and focuses on the mechanisms of radial transport.Electrophysiological mapping and intracellular injection of fluorescent dyes demonstrate that stem tissue is organized insymplastic subunits specialized in either longitudinal or lateral transport. Radial orientation, anatomical and physiologicalorganization, strong metabolic activities, relatively negative membrane potentials, and high capacities of uptake make the rays themost likely routes for symplastic xylem-to-phloem transport. Parallel apoplastic transport may occur through radial canaculesbetween the ray cells. The symplastic xylem-to-phloem transport includes a number of steps: (a) passage across thevessel/parenchyma interface, (b) transfer in the ray, and (c) delivery from the ray into the sieve tube/companion cell complex.Large contact pits in the vessel walls give access to the ray cells, by which the solutes are accumulated through substrate/protonco-transport. Dense pitting on the tangential walls and other ultrastructural features suggest preferential symplastic transport inthe radial direction. Auxiliary endo/exocytosis is under dispute. The transport step from the ray to the sieve tube/companion cellcomplex remains to be elucidated. In phloem-to-xylem transport, the unloading from the phloem along the stem is essentiallyapoplastic, but under specific conditions it may be symplastic. Further transfer to the xylem probably occurs via the symplasticroute through the ray. During radial transport, important metabolic interconversions take place into either transport or storagecompounds. In many trees, the metabolism of the ray cells undergoes cyclic, annual fluctuations. Complex season-bounddeposition/mobilization processes in the ray cells corresponding with seasonal changes in membrane permeability and cellularorganization, reflect a master-system designed to co-ordinate the C/N economy throughout the year.

Key words: Xylem-phloem exchange, radial transport.

INTRODUCTIONThe work of Stout and Hoagland (1939) and Biddulphand Markle (1944) established the phenomenon of solutetransfer from xylem to phloem and vice versa. However,our knowledge of the exchange between xylem andphloem is still very limited. Apart from work on legumes(Pate, Layzell, and Atkins 1979a; Pate, Layzell, andMcNeil, 1979*; Pate, Atkins, Herridge, and Layzell, 1981;Layzell and LaRue, 1982; Pate, 1986) and Triticum (Lam-bers, Beilharz, Simpson, and Dalling, 1982; Simpson,Lambers, and Dalling, 1982, 1983) dealing with fluxanalyses of organic compounds, systematic documenta-tion on xylem-phloem exchange of solutes in intactherbaceous plants is lacking. The physiological character-istics of the radial transfer have been described in depth

© Oxford University Press 1990

only for a few trees (Sauter, 1966a, b, 1971, 1980*, 1981a,b, c, 1982a, b, 1983, 1988).

Mineral uptake by roots, solute transport through thexylem, phloem loading and unloading, and the associatedlong-distance transport and partitioning have been moreappealing and rewarding subjects for transport physiolo-gists. Moreover, transport physiology of roots and leavescan be studied without perturbation or only with minordamage to relatively large and structurally uniformorgans. Work on radial transport is technically moredifficult. It requires major surgery to separate the minutetissues responsible for xylem-phloem exchange from abulk of other tissues with the risk of results which are notvery representative for the in vivo situation. Therefore,

632 Van Bel—Xylem-Phloem Exchange

much knowledge on radial transport has been obtainedusing indirect approaches.

This paper aims to link anatomical and physiologicalaspects of the xylem-phloem exchange studied at thecellular, tissue and whole-plant level in plant physiology,horticulture and silviculture and focuses on the mechan-isms of radial transport. Earlier reviews on radial trans-port have laid more emphasis on the metabolism of raycells (H611, 1975) and the seasonal metabolic changes inrelation to radial flux rates in trees (Sauter, 1982/)). Thepresent review will be restricted to the most elaboratexylem-phloem exchange, the radial transport of solutes inthe dicotyledonous stem, with occasional reference to thetransport events in conifers. The exchange of solutes inpetioles and leaf veins is beyond the scope of the review,though solute exchange between xylem and phloem issubstantial in these organs (McNeil, Atkins, and Pate,1979; Vogelmann, Dickson, and Larson, 1985; Simpson,1986; Van der Schoot, 1989).

As for the solutes transported, the paper will dealprimarily with the xylem-to-phloem transport of organicN-compounds which are synthesized in the roots in largequantities (Bollard, 1960; Pate, 1974) and with thephloem-to-xylem transport of photosynthates.

IMPORTANCE OF XYLEM-PHLOEMEXCHANGE FOR SOLUTEPARTITIONING IN INTACT PLANTSIt has become clear that xylem-to-phloem transport is animportant determinant of the carbon and nitrogen distri-bution within the plant (Pate et ai, 1980; Simpson, 1986).A simple experimental system suffices to demonstrate thesignificant contribution of xylem-to-phloem transport tosolute partitioning between the metabolic sinks (Van Bel,1984). Comparison of the partitioning of the xylem trans-port marker inulin carboxylic acid and the unnaturalamino acid analog a-aminoisobutyric acid allowed quan-tification of the xylem/phloem import ratio of each indi-vidual leaf. For instance, all a-aminoisobutyric acidfound in a mature leaf (leaf number 5) had been importedvia the xylem, whilst the apex (leaf number 13) acquiredonly 5% of this amino acid through the xylem. Appar-ently, the nutritional demands of the apical sink leaveswere almost fully met by phloem import of solutesoriginating from xylem-to-phloem transport in the stem.

More sophisticated modelling of xylem-to-phloemtransport of organic carbon and nitrogen in intact plantshas been produced by Pate and coworkers (Pate et al.,1979a, b; McNeil et al., 1979; Pate et al., 1981; Layzell andLaRue, 1982). Collection of xylem and phloem sap fromLupinus albus enabled the carbon and nitrogen fluxes to beanalysed. Xylem-to-phloem transport in the stem of Lupi-nus was found to provide the shoot apices with 60%, thefruits with 70% and the nodulated roots with 23% of thenitrogen they received through the phloem (Pate et al..

19796). In soybean, xylem-to-phloem transport was calcu-lated to be responsible for the import of 35% to 52% fruitN (Layzell and LaRue, 1982).

Whole-plant studies in Lupinus (Pate et al., 1979a; b;1980) and Triticum (Simpson et al., 1982, 1983) revealed acontinuous cycling of nitrogen, mediated by xylem-phloem exchange, and provided a much more dynamicimpression of the nitrogen economy than appears frommere analysis of plant parts. The key role of xylem-phloem exchange in C/N cycling and budgetting in herba-ceous plants has been reviewed elsewhere (Pate et al.,1980; Simpson, 1986; Pate, 1986).

Trees and, in particular, the deciduous trees of thetemperate zone, rely on xylem-phloem exchange morethan any other group of plants, since radial transport is anobligatory part of their survival strategy. Rays function asstorage organs, to or from which materials are radiallyimported or exported depending on the season. Seasonalfluctuations in storage and mobilization occur in decidu-ous forest (e.g. oak-McLaughlin, McConathy, Barnes,and Edwards, 1980; willow—Sauter, 1981a; 1988;poplar—Bonicel, Haddad, and Gagnaire, 1987), in fruit(e.g. peach—Stassen, Stindt, Strydom, and Terblanche,1981; apple—Titus and Kang, 1982; walnut—Deng,Weinbaum, and DeJong, 1989a; Deng, Weinbaum,DeJong, and Muraoka, 19896), trees and shrubs (e.g.kiwi—Ferguson, Eiseman, and Leonard, 1983) as well asin evergreen Gymnosperms (e.g. Picea—H611, 1984;Pinus—Smith and Paul, 1988) and Angiosperms (e.g.lemon—Kato, 1986; olive—Drossopoulos and Niavis,1988a, b).

THE PRESUMPTIVE PATH OFXYLEM-PHLOEM EXCHANGEOrganic N-compounds produced by the roots are takenup from the xylem stream along the vascular path.Autoradiographs showed a heterogeneous distribution of14C-labelled amino acids fed to detached shoots; mostlabel was retained by the nodes (Pate, Gunning, andMilliken, 1970; McNeil et al., 1979). Likely reasons forthis are that the vessel surface is enlarged by vascularanastomoses in the node and that, with the exception oflegumes (Kuo, Pate, Rainbird, and Atkins, 1980), onlynodes contain xylem transfer cells, particularly in thedeparting traces (Pate et al., 1970; Gunning, Pate, andGreen, 1970). The transfer cells are disproportionallyactive in withdrawal from the vessels (Pate and O'Brien,1968; Pate et al., 1970). In species without transfer cells inthe stem, unspecialized internodal xylem parenchyma cellsare also capable of appreciable uptake from the vessels(Van Bel, 19786).

Ready transfer from xylem to phloem has been found(Urquhart and Joy, 1982; Pate, Peoples, and Atkins, 1984;Vogelmann et al., 1985). Solutes which are poorlyabsorbed by the xylem parenchyma hardly arrive in the

Van Bel—Xylem-Phloem Exchange 633

phloem (Rainbird, Thome, and Hardy, 1984; Yoneyama,1984; Vogelmann et al., 1985), which shows that escapefrom the vessels and appearance in the phloem arecorrelated. These observations are complemented by (mi-cro)autoradiographs of stems through which 14C-aminoacids were translocated administered to the xylem vessels.The pictures illustrate that the main avenue for radialtransfer from xylem to phloem is through the rays(McNeil et al., 1979; Dickson, Vogelmann, and Larson,1985; Vogelmann et al., 1985).

It is well-established that assimilates can escape fromthe sieve tubes and cross to the xylem (Swanson and ElShishiny, 1958; Eschrich, 1966; Peel, 1967; Hardy andPossingham, 1969). Part of the evidence is autoradiogra-phic: 14C-photosynthate produced in the leaves and initi-ally transported by the phloem, rapidly shows up in thexylem (Webb and Gorham, 1965; Eschrich, 1966). Explicitmicro-autoradiographic evidence on the route of radialmovement is scarce (Ziegler, 1965; Langenfeld-Heyser,1987), but demonstrates unequivocally that the radialtrack runs through the rays.

The rays are radial plates of parenchyma cells in thevascular bundles of larger herbaceous and all woodydicotyledons. Their anatomical and physiological organi-zation seems to reflect specialization in xylem-phloemexchange (H611, 1975). If lateral transport occurs throughthe rays, radial solute transport includes at least threesteps: uptake from the xylem vessels by the contact raycells, cell-to-cell transfer through the rays, and deliveryinto the sieve tubes (Fig. 1). The structural and physiolog-ical features of the vessel/ray cell interface, the array of

ray cells and the interface between ray and sieve tube-companion cell complex will be examined in the followingsections.

T H E S T R U C T U R A L F R A M E O F R A D I A LT R A N S P O R TThe vessel/ray interface

It is expected (Sauter, 19826) that solutes from the vesselsreach the ray cells via the contact pits. These are extremelylarge pits between the ray cells and vessels. The thin,loosely woven or even partly open cellulosic network inthe pit (Siau, 1984) may give easy access to water andsolutes. This claim is substantiated by the observationthat the permeability of the secondary walls to lanthanumions was low, whereas the contact pit membranes exhib-ited a very high permeability to lanthanum (Wisniewski,Ashworth, and Schaffer, 1987a, b). Thus, the contact pitsconstitute the gates between vessel and apoplast of thexylem parenchyma.

Before entering the symplast, the solutes must pass theprotective layer, a peculiar deposit formed in the contactcells of many species after completion of the secondarywall. This tertiary layer is situated unilaterally against theparatracheal cell walls (e.g. Robinia; Czaninski, 1973) oralong the whole cell wall with a thicker deposit at thetracheal side (e.g. Ly coper sicon; Mueller and Beckman,1984). The protective layer is as electron-dense as theprimary pit walls and is also composed of primary pecto-cellulosic substances (Czaninski, 1977; Gregory, 1978;Mueller and Beckman, 1984). The occasional transfer cell-like projections of the protective layer at the contact pit

contactpit

interparen-cnyma pits

on thetangential

walls

T"\xylem vessel ray parenchyma sieve tube/

companioncell complex

FIG. 1. Simplified model of the presumptive radial route of xylem-phloem exchange. Solutes from the vessels move via the contact pits to the plasmamembrane boundary of the ray symplast after having crossed the protective layer. After transmembrane transfer, cell-to-cell displacement via theplasmodesmata brings the solutes to the vicinity of the sieve tube/companion cell complex. The nature of the path between ray and sieve tube/companioncell complex is uncertain. Materials moving from sieve tube to vessels follow essentially the same route in the opposite direction. In parallel with thesymplastic path, an apoplast continuum from vessel to sieve tube is available for the solutes not absorbed by the parenchymatous elements.


areas (Wooding and Northcote, 1965; Mueller and Beck-man, 1984; El Mahjoub, LePicard, and Moreau, 1984;Castro, 1985, 1986) may point to a special role of thecontact pits in solute transfer. The wall extensions arethought to intensify transmembrane solute transfer byproviding a larger membrane surface area for uptake(Pate and Gunning, 1972).

Though the protective layer is highly water-permeable(Wisniewski et al., 1987a, ft), one wonders why a protec-tive layer occurs at all. The initial postulate (Schmid,1965) that the layer protects the paratracheal cells againstlytic enzymes digesting the primary walls proved to beuntenable (Czaninski, 1973). At present, the involvementof the protective layer in the formation of tyloses (Foster,1967) is generally accepted. Recently, this view has beenchallenged by the suggestion that the layer may functionprimarily as a buffer against the diurnal oscillations ofhydrostatic pressure in the vessels (Van Bel and Van derSchoot, 1988). The primary pit walls may be too weak towithstand tensions generated under slightly negative hy-dropotentials in the vessels. The protective layer may,therefore, act to strengthen the pit membrane to preventbulging of the xylem parenchyma (Van Bel and Van derSchoot, 1988).

Where the radial contact cells are absent, the vessels areoften surrounded by a sheath of axial contact cells withlarge pits (Van der Schoot and Van Bel, 1989ft). The ratioof axial to radial contact cells varies with the plant species(e.g. in tomato the ratio is 65:35; Van der Schoot and VanBel, 1989ft). This ratio concurs with the observation that,in sugar maple, axial contact cells appear to have moresurface area contact with vessels than the ray parenchyma(Gregory, 1978).

All 'contact elements' (Braun, 1970) or 'vessel-associ-ated cells' (Czaninski, 1977) are characterized by a densecytoplasm with well-developed endoplasmic reticulumand numerous ribosomes, mitochondria and peroxisomesand few, if any, amyloplasts (Czaninski, 1977). Togetherwith the transfer cell-like protrusions in the broad pitareas (Wooding and Northcote, 1965; Mueller and Beck-man, 1984; El Mahjoub et al., 1984; Castro, 1985, 1986),the structural features of the contact cells indicate highmetabolic activities that could fuel massive transmem-brane transport. The homology in strategic location andultrastructure suggests a function for the vessel-associatedcells similar to that of companion cells in phloem trans-port (Czaninski, 1977).

The ray

Having arrived in the contact cells, the solutes maymove symplastically. The preferential direction of trans-port will be radial, as the tangential walls of the rayparenchyma are perforated by numerous plasmodesmata,aggregated in pit fields (Barnett, 1981). In vascular rays oftomato, the pit frequencies on the transverse, radial and

tangential walls are in the proportion of about 5:5:8,respectively (Van der Schoot and Van Bel, 1989ft). Thefrequency of plasmodesmatal contacts in the tangentialwalls of the ray parenchyma cells of poplar (8-0 plasmo-desmata /urn"2 covering 1-98% of the wall surface; Sauterand Kloth, 1986) are comparable to plasmodesmatalfrequencies of other cells known to be engaged in short-distance transport (Robards, 1976).

In trees, some radial rows (contact cell rows) containcells with giant pits where the rays border the vessels;other rows (isolation cell rows) lack cells with such'contact pits'. This differentiation in contact and isolationcell rows (Braun, 1967) represents a division of labour.Only the contact cells sensu strictu are engaged in theexchange of solutes with the vessels; the rest of the contactcell row is utilized for storage (Braun, 1967, 1970). Theisolation cells are primarily designed for radial transport(Braun, 1967, 1970).

For rapid radial transport, special adaptations may bepresent at the plasmodesmatal junctions in the rays.Sauter (1982ft) speculated on a mechanism for rapidsymplastic transfer by which solute vesicles are transferredfrom cell to cell in the tangential pit areas of the ray cells.Since endocytosis may contribute significantly to trans-membrane transfer in plant cells (Saxton and Breiden-bach, 1988; Steer, 1988), it is not inconceivable thatendo/exocytotic events play an important role in theradial trafficking of solutes. In tomato ray cells, plasmamembrane-originating vesicles were observed in the pitareas (Van der Schoot, 1989). In developing xylem ele-ments, similar vesicles produced by invagination of theplasma membrane were thought to be associated with cellwall deposition (Robards, 1968). It is more likely, how-ever, that the vesicles in mature ray cells are operating incell-to-cell transfer, as their frequency was 30 times higherin the pit areas than along the rest of the cell wall (Van derSchoot, 1989).

Radial intercellular canacules between the ray cells offera potential route for apoplastic flow driven by the transpi-ration (Preusser, Dietrichs, and Gottwald, 1961; Fengel,1965; Van der Schoot and Van Bel, 1989ft). The canaculesprobably originate from fusion of schizogeneously-formed intercellular spaces (Van der Schoot and Van Bel,1989ft). The apoplastic component of lateral transportmay be significant. This supposition is corroborated bythe radial movement of amino acids through the apoplast(Van Bel, 1974a, 1978ft). Lateral escape of alanine fromxylem vessels was reduced to 20% when tomato stemparts were wrapped in plastic to prevent transpiration(Van Bel, 1974a). Potentially important exchange betweenradial apoplast and symplast is indicated by the manyblind pits in the ray parenchyma walls orientated towardsthe canacules (Preusser et al., 1961; Fengel, 1965; Van derSchoot and Van Bel, 1989ft). The radial canacules may befunctionally homologous to the radial tracheids in coni-

fers, which are largely responsible for radial permeability(Liese and Bauch, 1967).

The role of the cambial zone in the radial transport isobscure. Perhaps, this tissue plays a special role in theradial transport owing to its meristematic character.

The ray I sieve tube interface

Unlike the plasmodesmatal frequencies in the minorvascular bundles of the exporting leaves (Gamalei, 1985,1988; Van Bel, Van Kesteren, and Papenhuijzen, 1988),the number of plasmodesmatal connections between thecells along the phloem transport path are poorly docu-mented. In contrast to the intense symplastic contactbetween sieve tube and companion cell, few plasmodes-matal connections exist between the sieve tubes andphloem parenchyma (Esau, 1969, 1973; Kollmann, 1973;Hayes, Offler, and Patrick, 1985).

It is doubtful whether plasmodesmatal connectionsbetween the parenchymatous phloem elements are evenlydistributed as some authors assume (Kollmann, 1973;Behnke, 1975). In Mimosa, the plasmodesmatal frequencybetween phloem parenchyma and companion cells waslow compared to the frequency between the phloemparenchyma cells (Esau, 1973). A similar plasmodesmatalconstriction in the symplastic path from the sieve tube toother phloem cells was found at the companion cell/phloem parenchyma interface in Phaseolus (Hayes et al.,1985) and in Ricinus (A.J.E. Van Bel and R. Kempers,unpublished results). Owing to the possible symplasticisolation, the sieve tube/companion cell complex may actas an independently functioning unit in dicotyledons.

In conifers, intense plasmodesmatal contact was ob-served between the sieve cells and the Strasburger cells inthe rays (Sauter, 1980a). These connections have a charac-ter similar to that of the sieve tube membrane/companioncell contacts in Angiosperms (Sauter, Dorr, and Koll-mann, 1976). Strasburger cells are, therefore, regarded ascompanion cell equivalents, though also on the basis ofmany other ultrastructural features (Sauter et al., 1976).The plasmodesmatal coupling between sieve cells, Stras-burger cells, and the 'common' ray parenchyma elements(Sauter et al., 1976) suggests a direct symplastic transportroute from sieve cell to ray in conifers.

T H E R A D I A L PATH AS AP H Y S I O L O G I C A L D O M A I NElectrophysiological mapping of the membrane potentialsof the cells in the conducting bundles of tomato internodes(where 90% of the xylem elements are alive; Van der Schootand Van Bel, 1989a) suggests that the ray constitutes asymplast domain. The term symplast domain was coined byErwee and Goodwin (1985) and denotes a functional unit ofcells created by symplastic isolation. A relation betweensymplastic discontinuity and electrical disparity logicallyfollows from the linear relationship between the diameter of


the plasmodesmatal path and the electrical cell-cell conduc-tance (Overall and Gunning, 1982).

Cell elements with similar membrane potentials wereoften grouped together in the internodal tissue of tomato(Van der Schoot, 1989). This electrical clustering mayreflect the existence of symplast domains in the stem, eachcharacterized by its specific electric potential. The ray cellsconstitute cellular plates of relatively negative membranepotentials ( — 50 to —70 mV) in a matrix of living fibreswith membrane potentials between - 2 0 and —30 mV(Van der Schoot, 1989). These values are close to those ofwood ray cells in poplar, where 50% of the membranepotentials was in the range between - 5 0 and - 9 0 mV(Himpkamp, 1988). The rays in tomato likely provide aphysiologically insulated path for symplastic radial trans-port (Van der Schoot, 1989) linking the paratrachealparenchyma ( — 70 to — 100 mV) and the external phloem( - 7 0 to - 8 0 mV). Both appear to be axial symplastdomains on the basis of membrane potential clustering.

The movement of intracellularly injected, membrane-impermeant fluorescent dyes labelling plasmodesmatal con-nectivity supports the existence of axial symplast domainsin tomato stems such as the sieve tube/companion cellcomplex (Van der Schoot and Van Bel, 1989c) and theparatracheal parenchyma (Van der Schoot and Van Bel,1990). Plasmodesmatal connectivity in rays by radial move-ment of fluorescent dyes has not been assessed satisfactorilyyet, since the lignified character of the walls and thethinness of the cytoplasmic layer impeded intracellulariontophoresis (Van der Schoot and Van Bel, 1990).

P H Y S I O L O G I C A L E V I D E N C E FORP A R A L L E L TWO-WAY T R A N S P O R TF R O M X Y L E M TO P H L O E MThe vascular architecture and physiological organizationindicate two parallel paths for transport from xylem tophloem: (a) an apoplastic path through the radial canacules,and (b) a symplastic path through an array of ray cells.

Irrespective of the route, the vessel solutes commencetheir radial transport via the highly water-permeablecontact pits. Thus the escape from the porous vessels(contact pits!) is primarily of a physical kind, namelydiffusion out of the moving solution into the adjoiningfree space. Subsequent active uptake by the xylem paren-chyma cells maintains a diffusion gradient between vesseland the adjacent apoplast continuum. Horwitz' calcula-tions (1958) predicted a linear relationship between thelogarithm of the solute concentration in the vessels andthe distance of solute movement as result of first-orderkinetics (with a diffusion constant or a first order chemicalreaction-rate constant).

Perfusing 14C-amino acids through tomato excisedinternodes indeed produced a logarithmic relationshipbetween the escape and the length of the stem (Van Bel,1974a, b; Van Bel, Mostert, and Borstlap, 1979). Escape


from the xylem vessels obeyed biphasic saturation kineticsplus a diffusional component (Van Bel et al., 1979). It isnot clear whether the biphasic active uptake from thevessels is due to carrier systems with different saturationkinetics (see for a review, Reinhold and Kaplan, 1984) orto the heterogeneous distribution of substrate in theapoplast from which the solutes are absorbed (Ehwald,Sammler, and Goring, 1973).

The most logical explanation for the escape kineticsseems that the biphasic kinetics represents active uptakeby the xylem parenchyma cells and the diffusional compo-nent reflects solute movement through the apoplast. Thisinterpretation is consistent with the parallel functioning ofapoplastic and symplastic radial transport. Circumstantialevidence for an apoplastic pathway in herbs are theimmense apparent free space of the xylem path, muchlarger than the volume of the vessels (Van Bel, 1978a) andthe 5-fold increase of lateral transfer induced by transpira-tion (Van Bel, 1974a).

The basal driving force for radial flow of water in thedirection of the stem periphery, however, may be the highosmolarity of the sieve tube contents. This could also betrue for tree branches and stems, where stomata areabsent. Phloem-to-xylem transport, therefore, probablyfollows a one-way track through the radial symplast, asthe driving force for apoplastic radial mass flow of wateris in the opposite direction.

XYLEM-TO-PHLOEM TRANSPORTTransfer from vessel to contact cellSelectivity of the amino acid escape from the vessels wasobserved (Van Die and Vonk, 1967; Hill-Cottingham andLloyd-Jones, 1968), before a mechanism of transport wasestablished. Later, carrier-mediated uptake by the contactcells was found for many amino acids (Van Bel and Vander Schoot, 1980; Van Bel, Van Leeuwenkamp, and Vander Schoot, 1981). Acidic amino acids are remarkablypoorly absorbed (Van Bel, 19786; Vogelmann et al.,1985). It is not clear how many carrier types are involvedin the amino acid uptake from the vessels. Experimentswith transport mutants of tobacco indicate that only twodifferent carrier systems (one for the acidic, one for theother amino acids) are responsible for amino acid uptakein plants (Borstlap, Schuurmans, and Bourgin, 1987).

Internodal cell clusters with high membrane potentials,like paratracheal parenchyma and rays, simultaneouslydisplay a high metabolic activity (Van der Schoot and VanBel, 1990). Furthermore, micrographs of stems treatedwith tetrazolium chloride indicating metabolic activity(Van der Schoot and Van Bel, 19896) have a strongresemblance to micro-autoradiographs of stems fed with14C-labelled amino acids (Dickson et al., 1985; Vogel-mann et al., 1985). The positive correlation betweenmetabolic activity, membrane potential and uptake rate issuggestive of high rates of active uptake into the vessel

contact cells. In this context, the excessively high ATP-concentrations in the xylem parenchyma of tomato maybe significant (Van Bel et al., 1981).

The proton-motive force as the drive of carrier-medi-ated amino acid uptake from the vessels was discovered byperfusing buffered solutions with and without organicsolutes through excised internodes (Van Bel and Her-mans, 1977; Van Bel and Van Erven, 19796). Substrate/proton cotransport matches the pH-dependence of theescape from the vessels (Van Bel and Hermans, 1977), asA pH is one of the components of the proton-motiveforce. The sequence of the pH-optima was in the order ofthe pi (isoelectric point) of the amino acids. According toKinraide and Etherton (1980), acidic amino acids need tobe associated with two protons, whereas neutral aminoacids would only need one proton. Under physiologicalconditions, basic amino acids are always positivelycharged and, therefore, depend only on A ¥ for crossingthe plasma membrane. The fewer protons the amino acidsneed to be transported, the higher is the pH for optimaluptake, as with increasing pH, A pH decreasingly and A Wincreasingly contribute to the proton-motive force (VanBel et al., 1981). Selective sugar uptake from the xylemvessels is likely to be driven by the proton-motive force aswell, in view of its pH-dependent carrier kinetics andsensitivity to metabolic inhibitors (Van Bel, 1976; Van Belet al., 1979; Sauter, 1981a, 6, 1983; Himpkamp, 1988).

The promotive effect of light on amino acid uptake byinternode discs (Van Bel and Van Erven, 1979a) andexcised internodal xylem of tomato (Van Bel and Van derSchoot, 1980; Van Bel et al., 1981) was ascribed to anenhanced proton-motive force as a result of ATP-produc-tion probably via photophosphorylation (Van Bel et al.,1981). Appreciable photosynthetic activity was observedin the chloroplast-rich rays of Fouquieria (Nedoff, Ting,and Lord, 1985), Fagus (Larcher, Lutz, Nagele, andBodner, 1988) and Pinus (Langenfeld-Heyser, 1989). Thisassigns ray chloroplasts a function in the xylem-phloemexchange in assisting to maintain a proton-motive forcesufficient to keep the bulk of organic solutes within theradial symplast.

Complex H + /K+ exchanges accompany substrate up-take from the vessels (Van Bel and Van Erven, 1979a, 6),probably as result of H+/K+ charge compensations.Potassium ions are released into the xylem stream when asubstrate is taken up through proton symport (Van Beland Van Erven, 19796). In turn, the potassium concentra-tion of the xylem sap influences the rate of amino aciduptake (Van Bel and Van Erven, 1979a, 6; Van Bel andVan der Schoot, 1980). K+-concentrations lower than2-0 mol m~3 stimulate amino acid uptake in comparisonwith potassium-free controls, whereas K +-concentrations,higher than 20 mol m"3, do the reverse (Van Bel and Vander Schoot, 1980). In tomato, a high potassium concentra-tion (30 mol m"3) in the vessels decreased amino acid

withdrawal from the vessels and consequently diminishedthe xylem-to-phloem transport and the supply of theapical leaves with organic N (Van der Schoot, 1989). Theinhibitory action of potassium is ascribed to lowering thediffusion potential resulting in a decreased active uptakeof organic substrates (Komor, Rotter, and Tanner, 1977;Van Bel and Koops, 1985; Takeda, Senda, Ozeki, andKomamine, 1988).

Potassium also plays a role in the exchange of cationsattached to the negatively charged groups in the vesselwalls. This exchange interferes with the uptake of basicamino acids (Hill-Cottingham, and Lloyd-Jones, 1972;Van Bel, 1978/)) and is relevant to several fruit trees,where the basic amino acid arginine is the main organicN-carrier in xylem transport (Bollard, 1960).

Transfer from ray to sieve tube

How materials move from the ray to the sieve tube isunknown. The fragmentary anatomical data is not suffici-ent to support any proposal on ray-to-sieve tube transfer.A major objection against symplastic transfer from ray tosieve tube seems that the solutes have to move against aconcentration gradient (Warmbrodt, 1987). One mightspeculate, therefore, that an apoplastic step is required toenable accumulation into the sieve tubes. On the otherhand, transport against a concentration gradient may notbe incompatible with symplastic transfer (for arguments,see Van Bel et al., 1988).

The dramatic drop in the membrane potential betweensieve tube/companion cell complex ( - 90 to - 100 mV) andphloem parenchyma ( - 40 to - 50 mV) in vascular bundlesof tomato is indicative of the electrical isolation of the sievetube/companion cell complex from the adjacent cells (Vander Schoot and Van Bel, 1989c). After injection of fluores-cent dye into the sieve tube or companion cell, the proberemained within the complex (Van der Schoot and Van Bel,1989c). Both findings are compatible with symplastic dis-continuity between sieve tube/companion cell complex andphloem parenchyma (Esau, 1973; Hayes et al., 1985) whichis consistent with solute retrieval by the sieve tube/compan-ion cell complex from the apoplast.

Early work with Ricinus petioles provided the firstevidence for a sucrose/proton symport into the sieve tubesalong the translocation path (Malek and Baker, 1977).Direct evidence for proton-driven uptake is the sucrose-induced depolarization of the sieve tube plasma mem-brane (Wright and Fisher, 1981; Van der Schoot and VanBel, 1989c). The proton-motive force of the sieve tube/companion cell complex is thought to be substantial dueto the steep outside-inside pH gradient (Giaquinta, 1983and references therein). The electrogenic component ofthe membrane potential (about - 70 mV; Wright andFisher, 1981; Van der Schoot and Van Bel, 1989c) isgenerated by ATP-ases at the expense of ATP in the sievetube/companion cell complex (Peel, 1987).


The kinetics of sucrose uptake by isolated phloembundles of celery (Daie, 1987) and Cyclamen (Grimm,personal communication) demonstrate carrier-mediateduptake. The uptake parameters are close: Km 5-0 mol m""3

and 15 ftmol h " ' (gFW) ~' for celery and Km 5-2 mol m " 3

and 4-2 ^mol h" 1 (gFW)"1 for Cyclamen.

P H L O E M - T O - X Y L E M T R A N S P O R TTransfer from sieve tube to rayThe release of solutes from the sieve tube to the stemapoplast is controlled by the same pump/leak system thatdictates phloem loading (Minchin and Thorpe, 1987). Thepassive character of the delivery is indicated by enhancedappearance of ' 'C in the stem apoplast in the presence of/>-chloromercuribenzenesulphonic acid (Minchin, Ryan,and Thorpe, 1984). However, this criterion should be usedwith caution, as /J-chloromercuribenzenesulphonic acidhas been reported to block the sucrose carrier in theuptake (Delrot, Despeghel, and Bonnemain, 1980) or therelease of sucrose (Anderson, 1986) in leaves. Circumstan-tial evidence for photosynthate unloading into the apo-plast is that plasmolytic disruption of the plasmodesmatadid not inhibit the release of photosynthate (Minchin andThorpe, 1984; Hayes, Patrick, and Offler, 1987).

It is questionable whether passive photosynthate releasealong the stem is a general phenomenon, as phloemunloading induced by the stem parasite Cuscuta wasunder metabolic control (Wolswinkel, 1974). Treatmentwith 2,4-dinitrophenol and washing stem segments inmedia of 0 °C strongly reduced phloem unloading.

Rates of phloem unloading to the apoplast in stemshave been measured by following efflux of uC-labelledsubstrate (Minchin and Thorpe, 1984; Minchin et al.,1984) or by changes in the apoplastic pool size of sugars(Hayes and Patrick, 1985; Hayes et al., 1987). Given theconcentrations of 3 to 100 mol m~3 sucrose in the apo-plast (Patrick and Turvey, 1981; Minchin and Thorpe,1984; Hayes and Patrick, 1985) and 500 mol m" 3 in thesieve tubes, the passive efflux was computed to be between4 and 5 pmol c i r r 2 s"1 (Patrick, 1990). The passiverelease then accounts for 60 to 70% of the delivery fromthe sieve tubes (Hayes et al., 1985). This indicates theexistence of a parallel symplastic route of unloading.When the prevailing source/sink ratio favours net assimi-late storage in stems, unloading indeed seems to switch toa symplastic unloading route (Hayes et al., 1987).

Patrick (1990) speculated that the hydrodynamic plas-modesmatal properties change with the turgor relationsbetween sieve tube and surrounding phloem parenchyma.Pressure-regulated plasmodesmatal valves (Zawadzki andFensom, 1986; Cote, Thain, and Fensom, 1987) betweenthe sieve tube/companion cell complex and phloem paren-chyma would be consistent with seasonal apoplastic/sym-plastic transport shifts in sieve tube unloading along thepath. Alternatively, temporal closure of the plasmodesmata


may be obtained by plugging with osmiophilic substances(Kwiatkowski and Maszewski, 1985). Occlusion of theplasmodesmata could be performed by Ca2+-dependentcallose synthesis (Waldmann, Jeblick, and Kauss, 1988).

Reversible closure mechanisms would be of the utmostimportance for unloading in tree stems, where source/sinkmetabolism is strongly related to seasonal rhythms. Ac-cording to this line of reasoning, one might anticipate thatday/night oscillations in the hydrostatic potential of thestem tissue also influence the release from the sieve tubesand the intercellular traffic in the rays. Beside the openingstatus of the plasmodesmata, hydropotentials may steermembrane transport by sieve tube/companion cell com-plexes (Patrick, 1984; Wolswinkel, 1985) by affecting themembrane potential (Li and Delrot, 1987).

Transfer from ray to vessel

In spring, release from ray cells of trees into the vesselsinvolves massive delivery of amino acids and sugarsdeposited in the ray parenchyma during the previousmonths (Sauter, 1980*, 1981a, c, 1982a, 1983, 1988).During the rest of the year, only minute amounts ofassimilates arrive in the vessels (Sauter, 19806, 1981a,1982a, 1988). The retrieval systems of the ray cells appearto be so well-developed (Van Bel, 1976; Himpkamp, 1988)that hardly any sugars can escape under appropriatetemperature conditions (Sauter, 19816, 1983; Vogelmannet al., 1985). The same probably applies to amino acids(Hill-Cottingham and Lloyd-Jones, 1968; Van Bel, 19786;Dickson et al., 1985). Whilst resorption by the contact raycells undoubtedly represents a substrate/proton co-uptake(Van Bel and Van Erven, 1979a; Himpkamp, 1988), thenature of the release is less evident.

A major complication in the assessment of the leakagemechanism of sucrose is that sucrose is hydrolysed byapoplastic acid invertase and can be resorbed in the formof hexoses (Sauter, 19816, c, 1983). The nature of sucroseleakage in trees probably varies with the season (Sauter,1988). Passive leakage in winter may result from mem-brane damage due to repetitive freezing and thawing(Sauter, 19806). Sucrose leakage induced by 2 °C pro-ceeded more vigorously over a few days than in the 20 °C-controls (Sauter, 19806, 1982a). The leakage, however,was partly inhibited by p-chloromercuribenzoate andNaF indicating simultaneous facilitated exodiffusion viathe sucrose carriers (Sauter, 19806, 1982a). The conspicu-ous, well-timed burst of sucrose release in mid-spring wasascribed to active release of sucrose (Sauter, 1988). In thatperiod, exocytotic sucrose release may be required toattain a sufficient delivery into tree vessels (Sauter, 19826).

On the basis of comparison with amino acid transportin other tissues, it was concluded (Sauter, 1981a) that theamino acid efflux rates were unlikely to be caused merelyby exodiffusion. In parallel with the proposals for sugardelivery, it might be worthwhile to consider a differential

release mechanism for amino acids changing with the timeof the year.

C E L L - T O - C E L L T R A N S F E R IN T H E RAYS Y M P L A S T

On the basis of the arguments put forward in the previoussections, it is plausible that most of the xylem-to-phloemtransport and all phloem-to-xylem transport goes throughthe ray symplast. Symplastic transport accounted for theobserved flux rates of sugar from phloem to the ray cellsin Populus rather than cell-to-cell transfer via the apoplast(Sauter and Kloth, 1986). This conclusion was reachedthrough calculations on starch deposition in the rays andthe correspondingly required glucose supply (Sauter andKloth, 1986). In addition, the linear increase of starch inthe ray tissue over many weeks (Sauter, 1982a) is compat-ible with a structural limitation (i.e. the plasmodesmatalgates).

The broad margins of error in their calculations (Sauterand Kloth, 1986), however, do not allow assessment of thenature of the symplastic transport. According to Ziegler(1961), the transport velocities in rays are incompatiblewith the classic concept of diffusional transfer. Sauterhypothesized that vesicles, aggregated at the pit fields ofray cells (Sauter, 19826; Van der Schoot, 1989), areinvolved in the intensification of solute cell-to-cell trans-fer. It is not clear whether the vesicles originate from theendoplasmic reticulum (Sauter, 19826) or the plasmamembrane (Van der Schoot, 1989). Possibly, at least twotypes of vesicles occur: one (from the endoplasmic reticu-lum) containing enzymes engaged in the endo/exocytosisof metabolites enclosed by the second type (from theplasma membrane).

The polarity of the phosphatase activity—at the cam-bium-facing tangential walls during mobilization, at theopposite walls during deposition—suggests involvementin the transport of solutes. Sauter (19826) advancedstrong arguments in support of a key role of acid phos-phatase in the mobilization of starch. However, thepermanently high phosphatase activity at the contact pits(Sauter, 19666, 1967), even when starch is completelydissolved in the contact cells, indicates that the phospha-tase also may be involved in transmembrane transfer.Phosphatase activity at the contact area has been associ-ated with active sucrose secretion into the xylem vessel inspring (Sauter, 19826).

The frequent irregularities in the polarity of the phos-phatase activity (Sauter and Braun, 1968) have beenattributed to differential sink polarities in individual raysections (Sauter, 19826). This phenomenon, however,could also reflect a division of labour between the rays:some of them could be specialized in xylem-to-phloemtransport, others in phloem-to-xylem transport. Alterna-tively, one part of a ray could be designed for xylem-to-phloem transport, the other part for transport in the

opposite direction. The phosphatase test may be useful todetect such a differential transport through rays.

METABOLIC EVENTS IN THE RADIALPATHSolute transformation in the radial path determines thequantity and species of compounds available for transferand, hence, can be considered as one of the basic determi-nants of xylem-to-phloem exchange. Only aspects ofmetabolism relevant to xylem/phloem exchange will bebriefly discussed here.

After feeding 14C-compounds to the xylem vessels ofdetached shoots, tracheal sap was obtained by vacuumextraction and phloem sap by spontaneous bleeding (Pate,Sharkey, and Lewis, 1975; Sharkey and Pate, 1975). InSpartium, asparagine passed largely unchanged to thephloem whereas the 14C from aspartic acid or glutamineappeared in the phloem sap attached to other amino acidsor in a number of non-amino compounds (Pate et al.,1975). In Lupinus, certain 14C-labelled compounds (val-ine, asparagine, threonine, serine, citrulline, glutamine)were transferred rapidly in an unchanged form fromxylem to phloem. Of others (glycine, methionine, asparticacid, homoserine, glutamic acid and gamma-aminobu-tyric acid), the bulk appeared in the phloem in a variety ofcompounds (Sharkey and Pate, 1975). Rapid incorpora-tion of threonine and alanine into protein was observed inthe rays of Populus (Vogelmann et al., 1985). Whereasalanine was fully transformed, part of the threoninemoved unchanged to the phloem.

In trees, storage/mobilization and long-distance trans-port closely correspond according to annual cycles (see fora review, Sauter, 1982/?). The availability of amino acidsand sugars for radial transport is seasonally dependent asillustrated by inversely related seasonal fluctuations in freemetabolites in xylem and phloem and in protein, fat andstarch deposits in the rays (McLaughlin et al., 1980;Stassen et al., 1981; Titus and Kang, 1982; Sauter, 1982*;Ferguson et al., 1983; H611, 1984; Kato, 1986; Bonicel etal., 1987; Smith and Paul, 1988; Drossopoulos and Niavis,1988a, 6; Deng et al., 1989a, 6). The balance betweenstorage and mobilization undergoes seasonal changesdependent on factors which will be highlighted herebriefly.

DETERMINANTS OF SEASONALFLUCTUATIONS IN RADIAL TRANSPORTSauter (1966a, 19826) studied in detail the seasonal fluctu-ations of starch metabolism and distinguished six stagesof starch synthesis/breakdown in the xylem of Populus.The breakdown of starch followed a specific scenario(Sauter, 1966a). Starch deposition in summer and autumnfollowed the reverse order (Sauter, 1966a). The sequenceof events suggests that the pathway via contact cell andisolation cell row, the elements being cleared first and


filled last, is the preferential route of radial transfer, whichfunctions best when the starch obstacles have been re-moved.

Starch synthesis/breakdown in spring was temperature-dependent: starch was mobilized at temperatures lowerthan 5 °C and higher than 10 °C and deposited between5 °C and 10 °C (Sauter, 1967). The mobilization of proteinprobably is also temperature-dependent. In contrast tostarch, protein shows a two-peak mobilization in spring:the first one corresponding with the blossoming of themale catkins, the second with the sprouting of the vegeta-tive buds (Sauter, 1981a). The spatial and temporaldistribution of fat and protein deposition/mobilization intrees is an interesting target for future studies, as ourknowledge about this subject is very restricted.

Apart from the balance between storage and mobiliza-tion, membrane permeability of the ray cells is season-dependent. Sucrose uptake from the xylem vessels of Salixis subject to seasonal changes (Sauter, 1983). Duringsummer, this uptake is about four times higher than inmid-winter. Similar seasonal patterns were observed forglucose uptake by the xylem ray cells of Populus (Himp-kamp, 1988). The latter study analysed the factorsbringing about the seasonal changes in transmembraneflux. The pH-dependence of uptake indicated the involve-ment of sugar/proton cotransport solely between Apriland September. From October onwards, uptake kineticsdisplay a constant diffusional component starting todecrease in April, until the diffusional flux rate is fivetimes lower in July than in December. Active uptake isnegligible from December to March. In April, an activeuptake component rapidly develops, the Vm of which istwenty times higher between May and September than inthe mid-winter period. The A"m of the active uptakeremains constant throughout the year (Himpkamp, 1988).

The passive permeability of the plasma membraneseemingly is maximal during winter and early spring.Solutes which are mobilized during this period, leak enmasse into the vessels, the rate of which is accentuated bythe low level of active retrieval (Sauter, 19826).

The differential temperature effects in autumn andspring on enzyme activities involved in the deposition/mo-bilization of starch (Sauter, 19826) and the annual changeof polarity of the phosphatase activity in the ray cells(Sauter, 19666, 1967; Sauter and Braun, 1968) underlinethat radial transport is a process dependent on numerous,partly unknown metabolic determinants.

MODEL OF XYLEM-TO-PHLOEMTRANSPORTDistribution of 14C-amino acids in response to variousmanipulations allowed assessment of some determinantsof xylem-to-phloem transport in herbaceous plants (VanBel, 1984; Van der Schoot, 1989). These experimentsexploited the pecularity that, in detached shoots, the ray


system acts as a valve between the communicating vessels,xylem and phloem. It was concluded that xylem-to-phloem transport (a) occurs along the whole vascular pathwith preference for the nodes, (b) is inversely related to theflow rate in the vessels, (c) is dependent on the soluteconcentration in the vessels, (d) is affected by the K + -concentration in the vessels, (e) has an appreciable sym-plastic component as shown by the differential, reductiveeffect of metabolic inhibitors, (f) is dependent on storagein the ray parenchyma, as high amino acid pools preventuptake by the ray symplast and subsequent phloemloading. These parameters are used to construct asemi-quantitative two-way model of xylem-to-phloemtransport (Fig. 2). Essential for this model is that theproportion between apoplastic and symplastic radialtransport to the phloem in the stem changes with theendogenous and environmental conditions.

The results conform with partitioning of 14C-materialsapplied to the base of Populus shoots (Vogelmann et ai,1985). The acidic amino acids, poorly absorbed by thexylem parenchyma, arrived in the mature leaves via thexylem, while threonine, accumulated and partly metabol-ized by the ray cells, was transported to the apical leavesvia the phloem (Vogelmann et al., 1985). Alanine andsucrose were completely retained by the xylem paren-chyma of poplar.

ray cells with plasmodesmata ( = )

FIG 2. Tentative model of the two-way xylem-to-phloem transport(Van der Schoot, 1989). Symplastic path. (1) water and solute escapefrom the vessel via the contact pits, (2) membrane passage into the raysymplast domain, (3) exchange between cytoplasm and vacuoles orstorage metabolism, (4) transfer from cell to cell via plasmodesmata, (5)displacement to the sieve tube/companion cell complex, either symplasticor apoplastic. Apoplastic path. (1) diffusion of solutes not captured bythe ray cells in the direction of the sieve tube, (2) partial withdrawal bythe cells along the radial apoplast. (6) arrival in the sieve tube/compan-ion cell complex The diffusion gradient in the ray apoplast depends onthe vessel concentration C, and the uptake rates at '2' and '6'. respec-tively.

C O N C L U S I O N SIn conclusion, the determinants of xylem-phloem ex-change are:

(1) the flow rate in the transport channels. The rate ofmass flow in the vessels is related to the transpiration,in sieve tubes to the difference in loading and unload-ing rates at the extremes of the phloem system;

(2) the substrate concentration in the long-distance trans-port channels, which in turn is controlled by variousfactors;

(3) the substrate-specific carrier-mediated uptake in contactcells, ray cells, and sieve tube/companion cell complexes;

(4) the radial transport velocities through the symplasticand apoplastic paths;

(5) the metabolic conversions in the symplastic pathincluding deposition and mobilization of the reserves.The deposition/mobilization balance is dependent onseasonal changes in metabolic activity, enzyme activi-ties, organelle positioning, membrane permeabilityand retrieval capacity of the vascular symplast.

A C K N O W L E D G E M E N T SThe author is indebted to Drs John Patrick, MichaelErwee, and Chris van der Schoot for critically reading themanuscript.

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MINCHIN, P. E. H., RYAN, K. G., and THORPE, M. R., 1984.Further evidence of apoplastic unloading into the stem ofbean: identification of the phloem buffering pool. Journal ofExperimental Botany, 35, 1744-53.

and THORPE, M. R., 1984. Apoplastic phloem unloading inthe stem of bean. Ibid. 35, 538-50.

1987. Measurement of unloading and reloading ofphoto-assimilate within the stem of bean. Ibid. 38, 211-20.

MUELLER, W. C , and BECKMAN, C. H., 1984. Ultrastructure ofthe cell wall of vessel contact cells in the xylem of tomatostems. Annals of Botany, 53, 107-14.

NEDOFF, J. A., TING, J. P., and LORD, E. M., 1985. Structure and

function of the green stem tissue in ocotillo (Fouquieriasplendens). American Journal of Botany, 72, 143-51.

OVERALL, R. L., and GUNNING, B. E. S., 1982. Intercellular

coupling in Azolla roots. I. Electrical coupling Protoplasma,111, 151-60.

PATE, J. S., 1974. Uptake, assimilation and transport of nitrogencompounds by plants. Soil Biology and Biochemistry, 5,109-19.

1986. Xylem-to-phloem transfer—Vital component of thenitrogen-partitioning system of a nodulated legume. InPhloem transport. Eds J. Cronshaw, W. J. Lucas and R. T.Giaquinta. Alan R. Liss, New York, Pp. 445-62.

-ATKINS, C. A., HERRIDGE, D. F., and LAYZELL, D. B., 1981.

Synthesis, storage, and utilization of amino compounds inwhite lupin (Lupinus albus L.). Plant Physiology, 67, 37-42.

and GUNNING, B. E. S., 1972. Transfer cells. Annual Reviewof Plant Physiology, 23, 173-96.

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LAYZELL, D. B., and ATKINS, C. A., 1979a. Economy ofcarbon and nitrogen in a nodulated and non-nodulated (NO3-grown)legume. Plant Physiology, 64, 1083-8.

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SHARKEY, P. J., and LEWIS, O. A. M., 1975. Xylem tophloem transfer of solutes in fruiting shoots of legumesstudied by a phloem bleeding technique. Planta, 122, 11-26

PATRICK, J. W., 1984. Photosynthate unloading from seed coatsof Phaseolus vulgaris L. Control by tissue water relations.Journal of Plant Physiology, 115, 297-310.

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PEEL, A. J., 1967. Demonstration of solute movement from theextracambial tissue into the xylem stream of willow. Ibid. 18,600-6.

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PREUSSER, H.-J., DIETRICHS, H. H., and GOTTWALD, H., 1961.Elektronenmikroskopische Untersuchungen an ultradiinnenSchnitten des Markstrahlenparenchyms der Rotbuche—Fagussvlvatica L. Holzforschung 15, 65-75.

RAINBIRD, R. M., THORNE, J. H., and HARDY, R. W. F., 1984.Role of amides, amino acids, and ureides in the nutrition ofdeveloping soybean seeds. Plant Physiology, 74, 329-34

REINHOLD, L., and KAPLAN, A., 1984. Membrane transport ofsugars and amino acids. Annual Review of Plant Physiology,53, 45-83.

ROBARDS, A. W , 1968. On the ultrastructure of differentiatingsecondary xylem in willow. Protoplasma, 65, 449-64.

1976. Plasmodesmata in higher plants. In Intercellularcommunication in plants: studies on plasmodesmata. Eds B. E.S Gunning and A. W. Robards. Springer-Verlag, Berlin,Heidelberg, New York. Pp. 15-57.

SAUTER, J. J., 1966a. Untersuchungen zur Physiologie derPappelholzstrahlen. I. Jahresperiodischer Verlauf derStarkespeicherung im Holzstrahlparenchym. Zeitschrift fiirPflanzenphysiologie, 55, 246-58.

19666. Untersuchungen zur Physiologie der Pappelholz-strahlen. II. Jahresperiodische Anderungen der Phosphata-seaktivitat im Holzstrahlparenchym und ihre mogliche Bedeu-tung fur den KohlenhydratstofTwechsel und den aktivenAssimilattransport. Ibid. 55, 349-62.

1967. Der Einfluss verschiedener Temperaturen auf dieReservestarke in parenchymatischen Geweben von Baum-sprossachsen. Ibid. 56, 339-52.

1971. Respiratory and phosphatase activities in contactcells of wood rays and their possible roles in sugar secretionIbid. 67, 135-45.

1980a. The Strasburger cells—equivalents of the compan-ion cells. Berichte der Deutschen Botanischen Gesellschaft, 93,29-42.

19806. Seasonal variation of sucrose content in the xylemsap of Salix. Zeitschrift fur Pflanzenphysiologie, 98, 377-91.

1981a. Seasonal variation of amino acids and amides in thexylem sap of Salix. Ibid. 101, 399^11 .

19816. Sucrose uptake in the xylem of Populus. Ibid. 103,165-8.

1981c. Evidence for sucrose efflux and hexose uptake in thexylem of Salix. Ibid. 103, 183-7.

1982a. Efflux and reabsorption of sugars in the xylem. I.Seasonal changes in sucrose efflux in Salix. Ibid. 106,325-36.


— 19826. Transport in Markstrahlen. Berichte der DeutschenBotanischen Gesellschaft, 95, 593-618.

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— 1988. Seasonal changes in the efflux of sugars fromparenchyma cells into the apoplast in poplar stems (Populus-x canadensis 'robusta'). Trees, 2, 242-9.

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— DORR, I., and KOLLMANN, R., 1976. The ultrastmcture ofStrasburger cells ( = albuminous cells) in the secondary phloemof Pinus nigra (Hoess) Badoux. Protoplasma, 88, 31—49.

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VAN BEL, A. J. E., 1974a. The absorption of L-a-alanine and a-

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19786. Lateral transport of amino acids and sugars duringtheir flow through the xylem. Ph.D. dissertation, University ofUtrecht, the Netherlands.

1984. Method for quantification of the xylem-to-phloemtransfer of amino acids by use of 14C-carboxyl inulin as xylemtransport marker. Plant Science Letters, 35, 81-5.

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MOSTERT, E., and BORSTLAP, A. C , 1979. Kinetics of L-

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Ultrastructural indications for coexistence of symplastic andapoplastic phloem loading in Commelina benghalensis leaves.Differences in ontogenic development, spatial arrangementand symplastic connections of the two sieve tubes in the minorvein. Planta, 176, 159-72.

VAN LEEUWENKAMP, P., and VAN DER SCHOOT, C , 1981.

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1989c. Glass microelectrode measurements ofsieve tube membrane potentials in internodes and peti-oles of tomato (Solanum lycopersicum). Protoplasma, 149,144-54.

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VAN DIE, J., and VONK, C. R., 1967. Selective and stereospecific

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