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First published online January 7, 2009; 10.1104/pp.108.134791 Plant Physiology 149:1601-1608 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Phloem Loading Strategies in Three Plant Species That Transport Sugar Alcohols1,[C],[OA]Department of Plant Biology (E.J.R., E.A.R., V.A., R.T.) and Department of Horticulture (E.J.R., L.C.), Cornell University, Ithaca, New York 14853; Research and Development Division, Nunhems USA, Inc., Brooks, Oregon 97305–9625 (E.J.R.); Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (E.A.R.); and Plant Biotechnology Unit, Agro Aquaculture Nutritional Genomic Center, National Research Agriculture Institute, CRI-Carillanca, Temuco, Chile (V.A.)
Many plants translocate sugar alcohols in the phloem. However, the mechanism(s) of sugar alcohol loading in the minor veins of leaves are debated. We characterized the loading strategies of two species that transport sorbitol (Plantago major and apple [Malus domestica]), and one that transports mannitol (Asarina scandens). Plasmodesmata are abundant at all interfaces in the minor vein phloem of apple, and in one of two types of phloem in the minor veins of A. scandens. Few plasmodesmata are present in the minor veins of P. major. Apple differs from the other two species in that sugar alcohol and sucrose (Suc) are present in much higher concentrations in leaves. Apple leaf tissue exposed to exogenous [14C]sorbitol, [14C]Suc, or 14CO2 did not accumulate radiolabel in the minor veins, as determined by macroautoradiography. P. major minor veins accumulated radiolabel from [14C]Suc, [14C]sorbitol, and 14CO2. A. scandens minor veins accumulated 14C from [14C]Suc and 14CO2, but not from [14C]mannitol. We conclude that the movement of sugar alcohol from the mesophyll into the phloem in apple and A. scandens is symplastic and passive, but in P. major it involves an apoplastic step and is energized. We also suggest that apple leaves transport sorbitol in high concentrations to avoid the feedback limitation of photosynthesis that would result from driving passive movement of solute into the phloem with high levels of Suc alone. The loading pathways and the mechanisms by which hydrostatic pressure is maintained in the minor vein phloem of these species are discussed.
Many species transport sugar alcohols in the phloem (Ziegler, 1975  ; Zimmermann and Ziegler, 1975; Loescher and Everard, 2000; Noiraud et al., 2001b). Sorbitol (glucitol) is transported in the Plantaginaceae and Rosaceae, mannitol in the Apiaceae, Combretaceae, Oleaceae, and Plantaginaceae, and dulcitol (galactitiol) in the Celastraceae. Several roles have been suggested for sugar alcohols, including osmoprotection, quenching of reactive oxygen species, facilitation of boron transport, storage of reducing power, tolerance to salinity or drought, and involvement in plant pathogen interactions (Loescher and Everard, 2000; Williamson et al., 2002; Pommerrenig et al., 2007). In some plants, sugar alcohol concentrations in phloem sap may considerably exceed those of Suc.
As with Suc, sugar alcohols are synthesized in the mesophyll and subsequently loaded into the minor vein phloem for delivery to sink tissues. Although it is reasonable to assume that sugar alcohols are loaded by the same species-specific strategies as Suc, these strategies have not been well documented. In particular, there is a debate over the possibility that sugar alcohols load through the symplast (Moing et al., 1997
In general, solutes can enter the phloem either from the apoplast or through the symplast. Apoplastic loading is driven by the proton motive force and is capable of creating a steep uphill concentration gradient (Lalonde et al., 2004 In this regard it is important to note that the term loading is sometimes used to signify the use of energy to transfer solute into the phloem against a thermodynamic gradient, and at other times to describe any route or mechanism of entry into the phloem, including an entirely passive one by diffusion or bulk flow through plasmodesmata. In this article, we use the term loading to indicate both active and passive modes of entry, making a distinction between them when necessary.
Several methods have been used to distinguish between symplastic and apoplastic loading pathways for sugar alcohols. Sugar alcohol transporters, including a mannitol transporter from celery (Apium graveolens) leaves (Noiraud et al., 2001a
A functional strategy often used to link Suc transporter activity to loading is to test the effects of p-chloromercuribenzenesulfonic acid (PCMBS), a membrane-impermeant sulfhydryl-modifying compound, on phloem transport (Giaquinta, 1976
In another approach to establishing the loading route, Moing et al. (1997)
To overcome this difficulty, Nadwodnik and Lohaus (2008)
Nadwodnik and Lohaus (2008)
In this study we compared phloem-loading mechanisms in apple (like Prunus, a member of the Rosaceae), Plantago major, and Asarina scandens. Asarina spp. transport Suc, mannitol, raffinose, and stachyose (Turgeon et al., 1993
Apple The phloem in the minor veins of apple leaves consists of sieve elements (SEs), companion cells (CCs), and phloem parenchyma cells (PPs; Fig. 1A ). PP cells form a ring around the more internal SEs and CCs. This ring may be irregular, allowing direct contact of some CCs with bundle sheath (BS) cells. SEs, which are often in clusters of two or more, occupy the most central position in the veins and only occasionally abut the BS. In the smallest veins there is only a single cluster of SEs, but in larger veins there may be several, separate from one another and evidently derived from the confluence of smaller veins.
The ultrastructure of the SEs is as commonly described (Behnke and Sjolund, 1990 ), being almost devoid of internal contents and lined by parietal cytoplasm. Lateral sieve plates are commonly found between adjacent SEs. In some, but not all, SEs the walls are thick and convoluted internally (Schlag and Gal, 1996). CCs and PP cells are much larger than SEs. CCs usually have denser cytoplasm, with numerous mitochondria and ribosomes. They have relatively small vacuoles, whereas PP cells are more highly vacuolated and have fewer mitochondria. The most consistent feature that distinguishes the two cell types is the nature of the plastids. PP cells have chloroplasts that are much smaller than those of mesophyll or BS cells, but have well-defined granal stacks. The plastids of CCs have few, if any, visible thylakoids, although plastoglobuli are common. Although these features often can be used to tell one cell type from another, in a given section the various distinguishing features may not be visible. Plasmodesmata are a prominent feature of apple veins. They are found in electron micrographs with regularity (Fig. 1, B and C). The walls are generally thickened at the site of plasmodesmata. This thickening is less pronounced at BS:BS interfaces. The plasmodesmata at PP:PP and PP:CC interfaces are branched, usually bilaterally in a given section (Fig. 1, B and C), which means that they are more highly branched in three dimensions. The branches converge in a prominent central median cavity. The number of branches is approximately equal on either side of the median cavity (data not shown). Plasmodesmatal neck occlusions or constrictions were not observed. Where plasmodesmata-pore units link CCs and SEs, the walls are especially thick.
Plasmodesmata are most frequent at the BS:PP, PP:PP, and PP:CC interfaces (Table I
). This is consistent with a role for PP cells in the distribution of photoassimilate within minor veins (Turgeon and Ayre, 2005
Leaf discs of mature apple leaves were abraded with carborundum, exposed to solutions of either [14C]Suc, or [14C]sorbitol, washed, freeze dried, and autoradiographed (Fig. 2 ). Minor veins were not apparent in the autoradiographs, indicating that label did not accumulate in the phloem.
Since the absence of a vein image is a negative result, we considered the possibility that the radiolabeled solutions did not have adequate access to the interior of the leaf tissue. Therefore, a number of methods were used to facilitate uptake. Either the adaxial or abaxial surfaces were abraded with carborundum or sandpaper for different periods, resulting in a wide range of scouring levels from mild erosion of the cuticle to obvious disruption of leaf integrity. In other tests the adaxial epidermis, or the epidermis and one or more layers of mesophyll, was removed with a razor blade. Parallel experiments using the fluorescent tracer 6-carboxyfluorescein diacetate indicated that many of these treatments allowed access of solutions to the mesophyll and veins (data not shown). However, the results of all trials with radiolabeled solutions were uniformly negative: No dark vein images were obtained using either [14C]sorbitol or [14C]Suc. We also noted that no minor vein images were apparent at the cut edges of the discs although vein patterns are seen at the edges of leaf discs of apoplastically loading species, even if the tissue is unabraded, due to penetration of label into the cut surface (Eschrich and Fromm, 1994 ). Similarly negative results were obtained with abraded leaf tissue of several other members of the Rosaceae (data not shown).
A pattern of lesser radiolabel accumulation was observed in the autoradiographs that corresponded with larger veins (Fig. 2). In transverse sections of leaf tissue (Fig. 3
) it can be seen that the larger veins have broad BS extensions, composed primarily of nonliving sclerenchyma cells that extend almost to the upper and lower epidermal layers (Nikolopoulos et al., 2002
P. major
In P. major, the SEs are in the center of the vein and are surrounded by a single layer of alternating CC and PP cells that directly abut the BS (Fig. 1D). In larger minor veins, the SE-CC complexes are internal and are entirely surrounded by a layer of PP cells (data not shown). PP cells have relatively dense cytoplasm, numerous mitochondria, and small chloroplasts with starch grains. CCs have dense cytoplasm, numerous mitochondria, plastids with few internal membranes and no starch, and the vacuoles are usually smaller than those of PP cells. The abaxial PP cells, just below the CCs, are specialized as type B transfer cells (Gunning and Pate, 1969 Autoradiographs of abraded leaf discs floated on solutions of [14C]Suc or [14C]sorbitol exhibited distinct vein-loading patterns (Fig. 2). Leaf tissue exposed to 14CO2 in the same manner as for apple also consistently produced minor vein images in autoradiographs (Fig. 2).
The concentrations of transport carbohydrates (Suc, mannitol, raffinose, and stachyose) and the minor vein anatomy of A. scandens (Turgeon et al., 1993
Solute transport between plant cells occurs either through plasmodesmata or across the apoplast. Since Suc can enter the phloem in the minor veins of leaves by one or the other route, depending on species (Schulz, 2005 ; Turgeon and Ayre, 2005), it is reasonable to suspect that sugar alcohols have the same opportunities. Of course, the issue of hydrostatic pressure must be addressed because long-distance transport requires the generation of sufficient pressure in the phloem to drive bulk flow of solution through sieve tubes. In the case of plants that transport sugar alcohols, this pressure can be produced in at least three ways (Fig. 4 ). The first is by a thermodynamically active mechanism that uses the proton motive force to load sugar alcohol into the phloem, from the apoplast, against a concentration gradient (Fig. 4A). Second, the combined concentrations of sugar alcohol and Suc, as well as other transported solutes, may be high enough in the cytosol of adjacent cells to generate the requisite osmotic potential in the phloem by passive transfer through plasmodesmata (Fig. 4B). Third, active loading of Suc by polymer trapping could provide the motivating force for long-distance transport, allowing sugar alcohol and other types of solutes to enter the phloem passively, through plasmodesmata, and to be carried along in the transport stream (Fig. 4C). The data presented here indicates that these three possibilities are realized in the three species under study.
Several lines of evidence indicate that, in Plantago, loading is thermodynamically active and occurs from the apoplast, as in Figure 4A. Autoradiographs of leaf tissue exposed to [14C]Suc, [14C]sorbitol, or 14CO2 demonstrate radiolabel accumulation in minor veins. Compared to apple, the number of plasmodesmata between the cells of the minor veins is limited, consistent with the Gamalei (1989) designation of Plantago spp. as type 2, with relatively few plasmodesmata in the minor vein phloem. Although plasmodesmata are found at each interface along the loading route, this is true of all plant species, including those known to load Suc from the apoplast (Schulz, 2005; Turgeon and Ayre, 2005). It is reasonable to suspect that the plasmodesmata between the SE-CC complex and surrounding cells in apoplastic loading species are narrow enough to prevent Suc leakage back to the mesophyll. However, the size exclusion limit of plasmodesmata at this boundary in minor veins has not been measured in any species.
A thermodynamically active-loading mechanism in Plantago is also indicated by measurements of Suc and sorbitol concentrations. According to Nadwodnik and Lohaus (2008) In the case of apple, the anatomical evidence favors passive entry of Suc and sorbitol into the phloem, as in Figure 4B. Abundant plasmodesmata are present at every interface from mesophyll cells to the SEs, in numbers that greatly exceed those in the minor veins of P. major (Table I).
Apple leaf discs exposed to [14C]Suc or [14C]sorbitol do not accumulate radiolabel in minor veins. The appearance of white veins in the apple leaf autoradiographs (Fig. 2) corresponds to larger veins that have prominent BS extensions (Fig. 3). Since the sclerenchyma cells in the extensions are nonliving, they do not accumulate radiolabel. Radiolabel may be present in the phloem of these veins, but it constitutes such a small percentage of the vein volume (Fig. 3) that it does not produce an image. In any case, most loading occurs in minor veins and they have either small BS extensions or none at all. The minor veins occur in the areas of the autoradiographs between the white vein images. No dark vein images, which would indicate radiolabel accumulation, are visible in these areas even though all three sorbitol transporters cloned from apple leaves are localized to the phloem (Watari et al., 2004 We suggest that the role of Suc and sorbitol transporters in apple leaves is to retrieve sorbitol that leaks from phloem cells into the apoplast. It is also possible that transporters transfer into the phloem a small amount of Suc and sorbitol that has leaked from the mesophyll into the apoplast. To a degree this could be considered phloem loading, but it is fundamentally different from a true apoplastic loading mechanism that relies primarily, if not entirely, on transporters and concentrates Suc in the phloem.
Solute concentrations in the mesophyll cells of apple leaves also indicate that passive loading is feasible. The concentration of sorbitol, based on leaf weight of 303 g m–2, and a water content of 62% fresh weight of leaf tissue (L. Cheng, unpublished data), is 269 mM in apple (Cheng et al., 2005
It is also important to note that flux through plasmodesmata is driven specifically by solute concentrations in the cytosolic compartment of cells. Studies of Suc and sugar alcohol compartmentation by nonaqueous fractionation indicate that disproportionately high concentrations are found in the cytosol compared to the vacuoles of mesophyll cells (Voitsekhovskaja et al., 2006
Nonetheless, according to the data of Nadwodnik and Lohaus (2008)
Considering the different types of data now available—autoradiography of 14C-labeled compounds, microscopic analysis of the symplastic pathway, and solute concentrations—we feel reasonably secure in proposing a symplastic and passive mode of phloem loading in apple and peach. We suggest that this offers an explanation for the high concentrations of sorbitol transported in these plants. Sugar alcohols serve several functions, including quenching of reactive oxygen species, improved boron mobility, storage of reducing power, and salt/drought tolerance (Loescher and Everard, 2000
The evidence also strongly supports a passive mode of sugar alcohol entry into the minor vein phloem in A. scandens. Asarina spp. transport Suc, with smaller amounts of raffinose, stachyose, and mannitol. When abraded leaf discs are exposed to [14C]Suc, vein images are readily apparent in autoradiographs. However, when discs chosen randomly from the same abraded tissue samples are exposed to [14C]mannitol, the results are negative: no vein images are seen, even when autoradiograph exposure time is adjusted to account for differences in the amounts of radiolabel accumulated. The difference in autoradiographic results is not due to a trivial problem in the visualization of [14C]mannitol since leaf discs of celery floated on solutions of [14C]mannitol produce distinct vein images in autoradiographs (data not shown). The results on Asarina are consistent with those of Voitsekhovskaja et al. (2006)
It may seem unlikely that symplastic and apoplastic modes of loading can coexist in a single species given that symplastic transport requires plasmodesmatal continuity while that same continuity would result in a futile transport cycle in the apoplastic loading mode. However, Asarina spp. have two types of phloem in the minor veins (Turgeon et al., 1993
Although sorbitol is loaded energetically into CCs in Plantago, mannitol is apparently not loaded the same way into the transfer cells of Asarina, otherwise a vein image would have been visible in autoradiographs when leaf tissue was floated on the radiolabeled compound. It is more likely that mannitol enters the adaxial CCs of Asarina. These CCs are not transfer cells. Rather, they resemble intermediary cells, with the asymmetrically branched plasmodesmata typical of this cell type. However, the plasmodesmata are not as numerous as in plants that transport large quantities of raffinose and stachyose, such as Alonsoa (Turgeon et al., 1993
Symplastic continuity between the mesophyll and phloem would explain the failure of leaf discs of A. scandens to accumulate [14C]mannitol in the veins. Since mannitol has only half the mass of Suc, it diffuses through narrow pores more readily than Suc, perhaps explaining why the number of plasmodesmata is reduced. Since Asarina spp. also transport small amounts of raffinose and stachyose (Turgeon et al., 1993 In conclusion, evidence is presented that sugar alcohols are loaded into the minor vein phloem of different species in different ways, taking advantage of the various pathways and mechanisms that are available for the entry of small molecules into SEs. Macroautoradiography of leaf tissue following abrasion and exposure to 14C-labeled exogenous compounds, measurement of solute levels, and analysis of plasmodesmatal frequencies are powerful tools in dissecting the pathways and mechanisms involved.
Plant Material Actively growing branches were collected from field-grown, fruiting cv Gala apple (Malus domestica Borkh.) trees at Cornell Orchards in Ithaca, New York. Branches were recut under water and transported to the lab. Leaves for two of the three leaf disc experiments were collected from potted Gala trees. Asarina scandens (Cav.) Penn. leaves were collected from plants grown in a greenhouse in Metromix 360 (E.C. Geiger). Plantago major leaves were collected in the field, except in the case of 14C-transport and leaf disc uptake assays, where the leaves were from plants cultivated in a growth chamber.
Leaf tissue was fixed in 2% (v/v) glutaraldehyde, 2% (v/v) paraformaldehyde, in 70 mM sodium cacodylate buffer, pH 7.0, for 1 h at room temperature, washed in the same buffer, and postfixed in 1% (v/v) osmium tetroxide. The tissue was dehydrated in an acetone series and embedded in Spurr's epoxy resin (Electron Microscopy Sciences). Thin sections were stained with uranyl acetate and lead citrate, and observed under a CM10 transmission electron microscope at 80 KV (Philips Electronic Instruments). For analysis of plasmodesmatal frequencies, individual plasmodesmatal channels were counted only if they extended one-half the distance from the plasma membrane to the median cavity. Plasmodesmatal channel frequencies were calculated by the formula of Gunning (1978)
For studies of exogenous uptake of Suc or sugar alcohol, the adaxial surface of leaf tissue was abraded with carborundum powder (320 grit) or the adaxial epidermis was removed with a razor blade, as described in "Results." Discs were cut with an 8-mm diameter cork borer under water and washed in MES buffer (20 mM MES plus 2 mM CaCl2, pH 5.5, with NaOH). Randomized discs were transferred, abraded side down, to the surface of fresh MES buffer in plastic dishes and the buffer was then removed and replaced with a solution containing MES buffer and either [14C]Suc, [14C]sorbitol, or [14C]mannitol (each at 1 mM; 40 kBq mL–1). After 1 h of radiolabel uptake at room temperature, with continuous, gentle agitation, the discs were washed for 1 h in ice-cold MES buffer, with several changes, and flash frozen in liquid N2 or powdered dry ice. The frozen leaf discs were lyophilized in a Virtis freeze dryer on a cold stage at –30°C with the condenser at –60°C. Dried discs were pressed thin between stainless steel plates in a bench vise, affixed to card stock with double-sided tape, and autoradiographed with Kodak BioMax MR film.
For studies of radiolabel distribution following photosynthetic incorporation of 14CO2, leaves were exposed to the radiolabeled gas as described (Turgeon and Medville, 1998 Received December 22, 2008; accepted December 31, 2008; published January 7, 2009.
1 This work was supported by the U.S. Department of Agriculture (grant no. CSREES 2005–02485).  The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Robert Turgeon (ert2{at}cornell.edu).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.108.134791 * Corresponding author; e-mail ert2{at}cornell.edu.
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