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First published online April 2, 2004; 10.1104/pp.103.035287 Plant Physiology 134:1793-1802 (2004) © 2004 American Society of Plant Biologists Evidence for Symplastic Involvement in the Radial Movement of Calcium in Onion Roots1Department of Biology, University of Waterloo, Waterloo, Ontario, Canada, N2L G1 (C.A.)
The pathway of Ca2+ movement from the soil solution into the stele of the root is not known with certainty despite a considerable body of literature on the subject. Does this ion cross an intact, mature exodermis and endodermis? If so, is its movement through these layers primarily apoplastic or symplastic? These questions were addressed using onion (Allium cepa) adventitious roots lacking laterals. Radioactive Ca2+ applied to the root tip was not transported to the remainder of the plant, indicating that this ion cannot be supplied to the shoot through this region where the exodermis and endodermis are immature. A more mature zone, in which the endodermal Casparian band was present, delivered 2.67 nmol of Ca2+ mm–1 treated root length d–1 to the transpiration stream, demonstrating that the ion had moved through an intact endodermis. Farther from the root tip, a third zone in which Casparian bands were present in the exodermis as well as the endodermis delivered 0.87 nmol Ca2+ mm–1 root length d–1 to the transpiration stream, proving that the ion had moved through an unbroken exodermis. Compartmental elution analyses indicated that Ca2+ had not diffused through the Casparian bands of the exodermis, and inhibitor studies using La3+ and vanadate (VO43–) pointed to a major involvement of the symplast in the radial transport of Ca2+ through the endodermis. It was concluded that in onion roots, the radial movement of Ca2+ through the exodermis and endodermis is primarily symplastic.
The pathway whereby Ca2+ moves radially from the soil solution to the tracheary elements of a root has long been a subject of debate (for reviews, see Clarkson, 1991  ; White, 2001; White and Broadley, 2003). To reach the root stele (the location of the tracheary elements), an ion must pass through the epidermis, exodermis (if present), central cortex, and endodermis. Because in typical roots the walls of the epidermis and central cortex cells are permeable to ions, the current debate concerns the passage of ions through the endodermis and exodermis.
One idea is that the Ca2+ delivered to the xylem may move predominantly or entirely apoplastically. This has been considered by a variety of authors (White, 1998
A second idea is that the Casparian bands in the endodermis and exodermis are circumvented by a symplastic step. In this case, the overall radial movement of Ca2+ to the stele would show features of symplastic transport. In support of this idea, there are some reports that Ca2+ movement to the shoot is not correlated with the speed of the transpiration stream (Atkinson et al., 1992
A third idea, one that reconciles the opposing views on the pathway (apoplastic versus symplastic) of radial Ca2+ movement through the endodermis, is that entry into the stele occurs near the root tip where the endodermis is immature (Flowers and Yeo, 1992
In this study, the passage of Ca2+ from the soil solution into the transpiration stream of onion (Allium cepa) roots was studied with a view to answering two questions: (1) Does this ion move radially through an intact exodermis and endodermis, or is the ion provided to the plant by the root tip (a region devoid of Casparian bands)? (2) If the ion does pass through an intact exodermis and/or endodermis, is its pathway predominantly apoplastic or symplastic? Young, adventitious roots sprouted from bulbs were chosen for this study because these roots lack laterals, the formation and emergence of which leads to discontinuities in the Casparian bands of the endodermis and exodermis, respectively (Esau, 1940
Sites of Ca2+ Uptake and Axial Transport Along Onion Roots Adventitious roots sprouted from onion bulbs developed uniformly when grown in the favorable conditions provided. Such roots were without laterals, either emerged or in the form of primordia. The roots were divided into three anatomical zones of interest with reference to the maturation of the endodermis, early metaxylem vessels, and exodermis (Fig. 1 ). The tip zone was the apical 5 mm of the root where functional xylem and Casparian bands were absent. The young zone, 15 to 40 mm from the tip, had functional xylem and Casparian bands in the endodermis. The old zone, which began 100 mm from the root tip and extended to the root base, possessed functional xylem, and Casparian bands in all cells and suberin lamellae in most cells of both the endodermis and exodermis. Thus, passage cells were present in both of the latter layers. For the experiments, the tip or the central regions of the young and old zones were sealed into a treatment chamber (Fig. 2 ).
When 1 mM 45Ca2+ was applied to the tip zone, no measurable radioactivity was detected in the rest of the plant (Table I). During the 24 h treatment time, the root tips had grown an average of 3 mm, which resulted in a final length of 8 mm being treated. In some cases, Casparian bands had formed in the endodermis in the proximal part of the treated zone, but the early metaxylem was always immature. Otherwise, the anatomy of the relevant structures did not change during treatment. When the young zone was treated, radioactivity was detected in the plant parts proximal but not distal to the treated site. The amount of 45Ca2+ extracted from the plant was equivalent to a delivery to the transpiration stream of 2.67 nmol mm–1 treated root length (Table I). Treatment of the old zone resulted in transport of 0.87 nmol mm–1 treated root length (Table I). As was the case for the young zone, 45Ca2+ movement from the old zone was only in an upward direction (i.e. toward the shoot). No positive correlation between the amount of the ion transported and transpiration rate was evident (Table I).
Impermeability of Exodermal Casparian Bands to Ca2+ The data from the compartmental elution of 45Ca2+ from both intact and dissected segments (Fig. 3 ) fitted a triple exponential function (Fig. 4 ) with average half-times ranging from 47 to 66 s, 5.6 to 7.5 min, and 102 to 210 min corresponding to wall, cytoplasm, and vacuole, respectively (although the identity of the last compartment is not known with any certainty; Table II elution at 22°C). The amount of Ca2+ in the wall compartment of the intact segments (2.0 µmol g–1 segment fresh weight [fw]) was substantially smaller than that in the dissected segments (8.8 µmol g–1 segment fw), indicating that the exodermal Casparian bands are not freely permeable to the ion (Table II, Fig. 3). Identification of the cell wall compartment, critical for this study, was validated by results of elutions at 4°C. Here the efflux from the wall compartment was unaffected (average half-time of 63 s), but that from the next (cytoplasmic) compartment could not be distinguished from the slowest (vacuolar) compartment (Table II). The half-time of elution from the latter combined compartment was not significantly different from that of the vacuole at 22°C in either whole or dissected segments (Table II).
Effect of Inhibitors on Ca2+ Transport to the Stele In the young zone of the root, treatment with inhibitors substantially reduced the flux of Ca2+ to the stele, as measured by the amount of the ion appearing in the root exudate. Addition of 1 mM La3+ to the treatment chamber (Fig. 5 ) resulted in 73% less Ca2+ in the root exudate compared to the control. Similarly, prior treatment of the cells in the stele with VO43– fed into the transpiration stream resulted in a 73% inhibition of Ca2+ translocation (Table III). Neither inhibitor affected the volumes of exudates produced by the roots (Table III).
Onion proved to be an ideal species for testing the permeability of the endo- and exodermis to Ca2+ as the roots did not develop laterals and, therefore, the Casparian bands of these layers, once formed, remained intact. Moreover, these roots did not develop root hairs, facilitating a clear distinction of the wall compartment in compartmental elution experiments.
When 45Ca2+ was applied to the root tip, the only location in the root not invested with at least one complete Casparian band, no measurable amount was transported away in the transpiration stream. Perhaps this is not surprising as this zone lacked mature xylem vessels. The general apoplastic impermeability of the tip noted in other studies (Lüttge and Weigl, 1962
In young zones of onion roots (between 15 and 40 mm from the root tip), where the endodermis and early metaxylem vessels were mature (Fig. 1), radioactive Ca2+ moved to the shoot. In fact, the largest amount was transported from this zone (Table I). In this region, no suberin lamellae are as yet developed in endodermal cells (Barnabas and Peterson, 1992
In the most mature (old) zone of the root (greater than 100 mm from the root tip), Casparian bands were present in the endodermis as well as in the exodermis (Fig. 1). Despite the presence of two sets of Casparian bands on the radial path, this zone was capable of transferring Ca2+ to the stele (Table I). This ion did, therefore, pass through an intact, mature exo- and endodermis. The less efficient radial transport in the old zone (compared to that of the young zone) could be a consequence of the presence of suberin lamellae in both the endo- and exodermis, as similar results were previously obtained with marrow and barley (Harrison-Murray and Clarkson, 1973 From the above comparison of Ca2+ transport through various root zones it is clear that, in this study, the ion does not enter the stele apoplastically at the root tip where Casparian bands are not yet formed, nor apoplastically in older regions through discontinuities in the Casparian bands of the endodermis and exodermis brought about by lateral root production. Rather, Ca2+ moved through an intact endodermis and exodermis on its way to the stele.
In all zones tested, there was a consistent lack of Ca2+ transport toward the root tip, supporting the general view that Ca2+ is immobile in the phloem and is not circulated within plants (Marschner, 1995
The technique of compartmental elution was used to discern the path of Ca2+ as it moved through the mature exodermis, a layer with Casparian bands near the root surface. With this technique, it is imperative to identify the compartment of interest (i.e. the wall) correctly. In this study, when 45Ca2+ was eluted from either intact or dissected segments, three compartments were distinguished. The fastest eluting of these was identified as the cell wall based on a comparison of its half-time (about 1 min) with literature data (Drew and Biddulph, 1971
Having identified and characterized the wall compartment, it was possible to test the hypothesis presented in the introduction, namely that a smaller amount of Ca2+ eluted from the walls of the intact segments with sealed ends compared to the amount eluted from the dissected segments would indicate that the Casparian band is not freely permeable to Ca2+. (It is necessary to assume that the Donnan free space of the epidermal and outer exodermal walls is the same as that of the walls of the central cortex.) These results were, in fact, obtained in experiments run at 22°C and 4°C (Table II). The amounts of Ca2+ in the wall compartments based on weight (as reported in Table II) can be corrected for sample volumes by considering that the length of the intact segments treated was 2.0 cm (not 2.5 cm), and that the steles were removed from the dissected segments. Then the average ratio of the amount of Ca2+ eluted from intact to dissected segments at 22°C is 1:3.3, and is near the range of those obtained earlier (1:3.9 to 1:6.3) by Peterson (1987)
The experiments designed to discover how Ca2+ moved through the endodermis on its way to the stele entailed measuring the amounts of this ion in root exudates, a method that has been used previously. For example, barley roots actively exuded externally applied 45Ca2+ from young (30 mm from tip) and mature (60 mm from tip) zones (Halperin et al., 1997
In this series of experiments, distinguishing a predominantly apoplastic pathway from a symplastic one rests on the effect of inhibitors of membrane function on delivery of Ca2+ to the root stele. If the entire route is apoplastic, the inhibitors should have no effect. If it is symplastic, however, a sharp reduction in the amount of Ca2+ delivered is expected. For this study, the inhibitors were chosen to give maximum effects on the delivery of Ca2+ to the stele. According to the model of Clarkson (1991)
Treatment of onion roots with either La3+ or VO43– substantially reduced the amount of Ca2+ in the root exudate (Table III), providing unequivocal evidence that the majority if not all the Ca2+ delivered to the stele passed through membranes. Thus, at least one symplastic step in the radial path is indicated. Treatment of onion roots with La3+ resulted in a 73% inhibition of Ca2+ transport to the stele (Table III). This incomplete inhibition may reflect the complex mechanism of Ca2+ transport by roots. It is apparent that other classes of Ca2+ channels might be present in the plasmalemmae of roots (White and Davenport, 2002
The results of this study support the model of Clarkson (1991) It should be noted that this work concerns the endodermis in two stages of development, i.e. with Casparian bands (in the young zone) and with the addition of suberin lamellae in most but not all cells (in the old zone). Similarly, passage cells were always present in the exodermis. The question of Ca2+ movement through an endodermis (or exodermis) with tertiary walls and without passage cells could not be approached with this experimental material. It is most likely that in this study, Ca2+ movement into the old zone was predominantly apoplastic in the epidermis and central cortex and was through the cytoplasms of only the passage cells of the exodermis and endodermis. Such symplastic steps would not involve Ca2+ transport through plasmodesmata. The results of this study clearly show that in onion roots, most or all of the Ca2+ that enters the root stele moves through the symplast at some point(s). Due to the impermeability of the endodermal Casparian band to ions (see introduction) and of the exodermal Casparian bands to Ca2+ (this study), these layers should be included in any symplastic path.
Plant Material Adventitious roots of onion (Allium cepa L. cv Ebeneezer) were generated from bulbs kept for 12 d in vermiculite-filled pots in a greenhouse. The longest roots measured 16 cm and none had reached the bottoms of the pots. The bulbs were near the end of their storage time (6 months after harvest) and sprouted leaves as well as roots.
Zones to be treated with radioactive Ca2+ were established by following the pattern of maturation of the endodermis, exodermis, and early metaxylem in the roots (Fig. 1) using the methods of Brundrett et al. (1988
Radioactive Ca2+ in the form of a chloride salt (45CaCl2) was applied to specific zones of the root (Fig. 2). An entire onion with its intact root system was placed in a tray that had been lined with wet, absorbent paper. The root to be treated was carefully positioned in a plexiglass box divided by partitions to create a 15-mm-long treatment chamber, two narrow bordering chambers to trap any accidental leakage from the treatment chamber, and two flanking chambers to hold the adjacent parts of the root (Fig. 2). The root was sealed into place with a mixture of 90% lanolin and 10% wax (previously heated while mixed; Barrowclough et al., 2000
After 24 h, the radioactive solution was removed and the solutions in the chambers on each side of the treatment chamber were probed for radioactivity to monitor leakage. To measure the length of the treated segment precisely, the incubation chamber was filled with an aqueous solution of Toluidine blue O (0.05% w/v) for 5 min. After removal of dye, the experimental root was measured and divided into parts, i.e. the treated segment, the distal (apical) section, and the proximal (basal) section. All these parts, in addition to the bulb and the leaves, were heated at 500°C for 17 h, cooled, and the resulting ash made up to 5 mL with 0.2 N HCl. A similarly processed, entire root from an untreated plant was used as a control. Radioactivity (
Segments used to determine the permeability of the exodermal Casparian band were prepared according to the procedure of Peterson (1987)
Labeling and elution were performed following the method of Peterson (1987)
Each comparison (i.e. intact versus dissected) was replicated at least three times. Data were analyzed as previously described (Peterson, 1987 To verify the identity of the cell wall compartment, three replicates of an experiment were eluted at 4°C. For this trial, intact and dissected segments were initially incubated in the 1 mM radioactive Ca2+ treatment solution at 22°C for 17 h. At the end of this labeling period, segments were blotted and then eluted (as described above) at low temperature.
To distinguish between Ca2+ transport in the apoplast versus the symplast of the endodermis, young zones of the root (with Casparian bands in the endodermis but not in the immature exodermis) were tested. The effects of La3+ and VO43– on the amounts of Ca2+ in root exudates were assessed. For each replicate of a La3+experiment, 10 roots were excised from one onion bulb. Each root was cut obliquely under water to obtain the distal 6 cm (i.e. the part of the root that included the tip). Five of the roots were sealed into a plexiglass box as described above so that a 15-mm length in the central region of the young zone could be treated (Fig. 5). Bordering and flanking chambers were filled with 1 mM CaSO4 and a treatment solution of 1 mM LaCl3 and radioactive Ca2+ (as described above) was added to the treatment chamber. The remaining five roots were sealed into a second chamber and treated in the same fashion but without LaCl3.
The membranes of the cells in the stele (including the membranes of the stele side of the endodermis) were exposed to VO43– by introducing a solution of sodium orthovanadate (Na3VO4, Aldrich, St. Louis) into the transpiration stream. The inhibitor solution was prepared according to O'Neill and Spanswick (1984) The potential effects of both inhibitors on the process of root exudation were tested. In the case of La3+, roots were excised from an onion bulb as described above, and the proximal (cut) end of each root was inserted into a 100-µL microcapillary tube and sealed in place with sticky wax (Kerr). The entire root piece was immersed in a solution of 1 mM CaSO4 and 1 mM LaCl3. In the case of VO43–, the inhibitor was introduced into the root xylem as described above. Roots were then severed from the bulb and sealed at the distal ends with sticky wax. The proximal ends of the roots pieces were then sealed into 100-µL microcapillaries (as described above) and the roots immersed in 1mM CaSO4. Control (untreated) and inhibitor-treated roots were allowed to exude for 17 h, after which the volumes of the exudates were calculated from the lengths of fluid in the microcapillaries.
We thank Dr. Alan Bown (Brock University, ON, Canada) and Dr. Martin Canny (Australian National University, Canberra, Australia) for critically reading the manuscript, Dr. Wilfried Rauser (University of Guelph, ON, Canada) for helpful discussions, Dr. Jack Carlson (University of Waterloo, ON, Canada) for use of the scintillation counter, and Tasneem Mohamed (University of Waterloo, ON, Canada) for drafting Figures 2, 3, and 5. Received October 23, 2003; returned for revision January 15, 2004; accepted January 20, 2004.
1 This work was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to C.A.P. 
2 Present address: BIOS Agriculture, 2111 Lakeshore Road, P.O. Box 187, Ste-Anne-de-Bellevue, QC, Canada, H9X 3V9. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.035287. * Corresponding author; e-mail cpeterso{at}uwaterloo.ca; fax 519–746–0614.
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ABSTRACT
RESULTS
-emissions) in each plant part was measured with a liquid scintillation counter (Searle Analytic, model Mark III) after addition of scintillation liquid (Ecolite, ICN, Irvine, CA). Four replicates were included in each experiment. Data from the plant parts external to the treated root area were pooled and analyzed by Student's t test (2 tails, 3 types – two samples unequal variance). 
