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The pathways of calcium movement to the xylem

The pathways of calcium movement to the xylem Abstract Calcium is an essential plant nutrient. It is acquired from the soil solution by the root system and translocated to the shoot via the xylem. The root must balance the delivery of calcium to the xylem with the need for individual root cells to use [Ca2+]cyt for intracellular signalling. Here the evidence for the current hypothesis, that Ca2+ travels apoplastically across the root to the Casparian band which it then circumvents via the cytoplasm of the endodermal cell, is critically reviewed. It is noted that, although Ca2+ channels and Ca2+‐ATPases are present and could catalyse Ca2+ influx and efflux across the plasma membrane of endodermal cells, their transport capacity is unlikely to be sufficient for xylem loading. Furthermore, there seems to be no competition, or interactions, between Ca2+, Ba2+ and Sr2+ for transport to the shoot. This seems incompatible with a symplastic pathway involving at least two protein‐catalysed transport steps. Thus, a quantity of purely apoplastic Ca2+ transport to the xylem is indicated. The relative contributions of these two pathways to the delivery of Ca2+ to the xylem are unknown. However, the functional separation of symplastic Ca2+fluxes (for root nutrition and cell signalling) and apoplastic Ca2+ fluxes (for transfer to the shoot) would enable the root to fulfil the demand of the shoot for calcium without compromising intracellular [Ca2+]cyt signals. This is also compatible with the observed correlation between transpiration rate and calcium delivery to the shoot. Arabidopsis thaliana, barium, calcium, Casparian band, endodermis, strontium. Introduction Calcium (Ca) is an essential plant nutrient. It fulfils a variety of structural roles, and functions as counter‐cation for inorganic and organic anions in the vacuole (Marschner, 1995). In addition, the cation (Ca2+) is essential for cell division and expansion, and explicit perturbations in cytoplasmic Ca2+ concentration ([Ca2+]cyt) link specific environmental or developmental stimuli to their appropriate physiological responses (White, 1998, 2000). Calcium is required in large amounts, and the Ca content of healthy plant tissues generally exceeds 0.1–1% dry matter. Dicotyledeonous plants require more Ca in their tissues than do monocotyledonous plants (Islam et al., 1987), which has been attributed to a larger cation exchange capacity of their cell walls (Kirkby and Pilbeam, 1984). Plants acquire Ca primarily from the soil solution through the root system, and the shoot is supplied via the xylem. In an actively growing plant the Ca flux to the xylem is high. For example, a cereal seedling with a shoot/root FW ratio of 2 and a relative growth rate of 0.2 d−1 must translocate Ca at rates approximating 40 nmol h−1 g−1 FW root to maintain its shoot Ca content at 0.1% dry weight (White, 1998). The root must balance this delivery of Ca to the xylem with the necessity for individual root cells to use [Ca2+]cyt for intracellular signalling (White, 1998; Kiegle et al., 2000b). A low (submicromolar) [Ca2+]cyt must be maintained in all root cells and [Ca2+]cyt must increase rapidly when challenged by appropriate stimuli. These properties may be compromised by high nutritional Ca2+ fluxes through root cells unless they can be controlled exquisitely. In this article the possible mechanisms by which the root might effect xylem Ca loading, without compromising cell signalling, are discussed. A particular emphasis is placed on the pathways of Ca2+ movement through the root to the xylem. Root anatomy and the structure and development of the endodermis The root is composed of many different cell types. Each cell type appears specialized to specific tasks (Clarkson, 1991; Maathuis et al., 1998). It is commonly suggested that the outer cell layers of the root, the epidermis and cortex, are involved primarily in the acquisition of water and mineral nutrients. These are separated from the cells of the stele, which are devoted to the loading, unloading and long‐distance transport of solutes in the xylem and phloem, by the endodermal cell layer (Fig. 1). The part of the root outside the plasma membrane is termed the apoplast. This includes cell walls, intercellular spaces and the lumena of tracheary elements. The interconnected cytoplasm of root cells is termed the symplast. In principle, solutes may reach the xylem either symplastically, by entering root cells and moving from cell to cell through plasmodesmata, or apoplastically, without traversing a single plasma membrane. However, in the mature root, an hydraulic separation of cortical and stelar apoplasts is imposed by the presence of an extracellular structure termed the Casparian band. This structure, which is present on the anticlinal (transverse and radial longitudinal) walls of endodermal cells, is present in all roots of vascular plants and is thought to act as a barrier to the apoplastic movement of solutes. (There appears to be a single exception to this statement. An endodermal Casparian band was not found in the roots of Lycopodium: Damus et al., 1997.) A Casparian band of some description is present throughout the root, including the regions that are considered most permeable to water and solutes, except for a few millimetres at the extreme root tip. The endodermis develops in three stages (Fig. 1; Esau, 1965; Clarkson and Robards, 1975; Peterson and Cholewa, 1998; Schreiber et al., 1999). Initially, a Casparian band is deposited within the transverse and radial longitudinal walls of the endodermal cells (State I), which becomes firmly attached to the plasma membrane of these cells. The Casparian band is composed primarily of lignin, but also contains some suberin (Schreiber et al., 1999). All cells in the endodermis develop a Casparian band approximately synchronously, following cell elongation and coincident with (or slightly prior to) the maturation of the protoxylem (Esau, 1965; Peterson and Lefcourt, 1990). At a variable distance from the apex, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II). This event frequently coincides with the emergence of lateral roots. The layers of suberin create a lamellar structure that isolates the endodermal cell protoplast from the apoplast and subsequently becomes buried by the deposition of lignified, carbohydrate cell walls (State III). These latter stages in the development of the endodermis proceed more rapidly in cells near the phloem compared to those near the xylem and ‘passage cells’, which remain in State I whilst those around them proceed to State III, can frequently be observed. It is speculated that passage cells are important in the transfer of ions to the stele in mature roots (Peterson and Enstone, 1996), because they become the only cells to expose a plasma membrane to the external solution (and therefore capable of ion uptake) when the epidermis and cortex die. The presence of suberin lamellae is thought to prevent endodermal cells from taking up solutes from the apoplast, but it is not thought to influence solute movement within the apoplast (Peterson and Cholewa, 1998). Fig. 1. View largeDownload slide Schematic views of the development of the endodermis and its hypothetical impact on the pathway of calcium movement to the xylem (Clarkson, 1993). Initially, the Casparian band develops as a modification of the anticlinal (transverse and radial longitudinal) walls between endodermal cells (State I). This is assumed to block apoplastic (cell wall) movement of calcium to the xylem, and to force the calcium destined for the xylem to enter the root symplast, through Ca2+ channels in the accessible plasma membrane of the endodermal cell. It is then assumed that this symplastic Ca2+ is pumped into the stelar apoplast by Ca2+ ATPases in the plasma membranes of cells within the stele. Subsequently, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II), and the endodermal cell becomes buried by the deposition of tertiary cell walls (State III). The deposition of suberin lamellae isolates the endodermal cell protoplast from the apoplast, preventing Ca2+ influx to endodermal cells and, thereby, calcium transport to the xylem. Fig. 1. View largeDownload slide Schematic views of the development of the endodermis and its hypothetical impact on the pathway of calcium movement to the xylem (Clarkson, 1993). Initially, the Casparian band develops as a modification of the anticlinal (transverse and radial longitudinal) walls between endodermal cells (State I). This is assumed to block apoplastic (cell wall) movement of calcium to the xylem, and to force the calcium destined for the xylem to enter the root symplast, through Ca2+ channels in the accessible plasma membrane of the endodermal cell. It is then assumed that this symplastic Ca2+ is pumped into the stelar apoplast by Ca2+ ATPases in the plasma membranes of cells within the stele. Subsequently, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II), and the endodermal cell becomes buried by the deposition of tertiary cell walls (State III). The deposition of suberin lamellae isolates the endodermal cell protoplast from the apoplast, preventing Ca2+ influx to endodermal cells and, thereby, calcium transport to the xylem. A symplastic pathway for calcium movement to the xylem The immediate and substantial drop in root pressure upon injury of the endodermis indicates that the Casparian band is the main barrier to the radial movement of ions across the root (Peterson et al., 1993; Steudle et al., 1993). Further, it has been proposed that Ca2+cannot enter the stele via the apoplast when the Casparian band is present (Clarkson and Robards, 1975; Clarkson, 1984, 1991, 1993; Marschner, 1995). This view is based on (i) the hydrophobic chemistry of the Casparian band, (ii) the rapid penetration of divalent cations (such as Ca2+ and Sr2+) and of cell impermeant tracers (UO2+2, La3+, hydrophilic dyes) into the cortex but not the stele of plant roots and (iii) the observation that Ca2+ delivery to the xylem is increased in regions of the root where the Casparian band is discontinuous or ruptured. Calcium delivery to the xylem is maximal in the apical zone of the root (Fig. 2), which comprises both immature and recently‐matured root cells. In this region, endodermal cells possess a Casparian band (State I). Although there is no direct evidence that either lignin or suberin are effective barriers to the movement of water and dissolved solutes (Schrieber et al., 1999), it is frequently assumed that these Casparian bands are impermeable to Ca2+ and, therefore, that Ca2+ must bypass the Casparian band symplastically prior to its delivery into the xylem (Fig. 1). It is further assumed that, since Ca2+ mobility in the symplast is restricted by low [Ca2+]cyt, most radial movement of Ca across the root will occur through the apoplast up to the Casparian band. However, it should be noted that Ca2+ is only a small fraction of the total cytoplasmic Ca pool and Ca chelates might move symplastically. Since the shortest symplastic route that circumvents the Casparian band is through the cytoplasm of the endodermal cell, it is argued that Ca2+ will utilize this pathway to minimize any compromise of [Ca2+]cyt signalling mechanisms (Clarkson, 1984, 1993). Upon the deposition of suberin lamellae in the endodermis (State II and III), Ca delivery to the xylem is severely restricted, even though the endodermal cells are still symplastically connected to the cortex and stele by functional plasmodesmata. This appears to confirm the absence of a symplastic pathway for Ca movement between the cortex and stele. The observation that Ca movement to the xylem decreases as endodermal cells become inaccessible from the apoplast is held to support the view that Ca destined for the xylem enters the symplast exclusively through endodermal cells. In basal regions of the root some Ca may reach the xylem through the apoplast as lateral roots emerge. During lateral root formation, the endodermal cells divide and the newly formed radial walls lack a Casparian band (Peterson and Lefcourt, 1990). However, Casparian bands are deposited at the base of lateral root primordia and rapidly become continuous with those of the endodermis of the parent root. Similarly, although the endodermal Casparian band may lose its function as an apoplastic barrier when roots undergo secondary (thickening) growth, this occurs only after it is replaced by the periderm (Esau, 1965; Weerdenburg and Peterson, 1984). In the roots of many plant species, particularly when grown in soil, an exodermis (hypodermis) develops that has both Casparian bands and suberin lamellae with chemical compositions and properties similar to those of the endodermis (Perumalla et al., 1990; Peterson and Perumalla, 1990; Damus et al., 1997; Schreiber et al., 1999). However, the integrity of the exodermal Casparian band is disrupted by the emergence of lateral roots, and its development is patchy, absolutely dependent upon environmental conditions (it does not form readily in plants grown hydroponically) and frequently subsequent to the suberization of the endodermis (Enstone and Peterson, 1992, 1997, 1998). Thus, in most cases, a complete Casparian band in the exodermis will be limited to regions where Ca delivery to the xylem would be minimal even in its absence, and so this structure is unlikely to influence Ca movement to the xylem. Consistent with this view, Zimmermann and Steudle (1998) observed that the transport to the xylem of the apoplastic dye PTS (trisodium 3‐hydroxy‐5,8,10‐pyrene‐trisulphonate) was not affected by the presence of an exodermal Casparian band. A scheme for Ca delivery to the xylem based on exclusive Ca2+ transport through endodermal cells is found in many textbooks (Clarkson, 1991; Marschner, 1995). In this scheme, Ca2+ is considered to travel apoplastically across the root to the Casparian band. To circumvent the Casparian band, it is proposed that Ca2+ enters the cytoplasm of the endodermal cell through Ca2+‐permeable channels. It is then actively effluxed from the symplast by the plasma membrane Ca2+‐ATPases or Ca2+/H+ antiporters of cells within the stele. In theory, the necessity for Ca2+ to traverse the plasma membrane of endodermal cells would allow the root to control the rate and selectivity of Ca transport to the shoot. The selectivity of the apoplastic route, which is determined by the ion exchange properties of the cell wall, is minimal. However, by diverting the cation flow through the cell, transport proteins in the cell membranes can selectively catalyse the movement of Ca2+ to the xylem (Clarkson, 1991). This could benefit the plant by restricting the movement of toxic cations to the shoot. However, several lines of evidence suggest that this simple scheme might be incorrect. In the next section the thermodynamic and kinetic feasibility of the symplastic transport pathway will be assessed. Then the apparent absence of selectivity or competition between divalent cations for transport to the shoot (both of which are characteristics of protein‐mediated transport pathways) will be considered. Fig. 2. View largeDownload slide The profile of calcium translocation to the shoot along the seminal root of marrow (Cucurbita pepo L.), and its relationship with the development of the endodermis. Calcium translocation is maximal in the root apical zone, where the endodermal cells possess a Casparian band (State I endodermis) and xylem vessels first become fully conductive, and declines as the endodermal cells become increasingly suberised (State II endodermis). Results were obtained by enclosing short (3.5 mm) sections of seminal roots in flow cells containing 0.15 mM Ca2+ labelled with carrier‐free 85Sr for 6 h (Harrison‐Murray and Clarkson, 1973). Fig. 2. View largeDownload slide The profile of calcium translocation to the shoot along the seminal root of marrow (Cucurbita pepo L.), and its relationship with the development of the endodermis. Calcium translocation is maximal in the root apical zone, where the endodermal cells possess a Casparian band (State I endodermis) and xylem vessels first become fully conductive, and declines as the endodermal cells become increasingly suberised (State II endodermis). Results were obtained by enclosing short (3.5 mm) sections of seminal roots in flow cells containing 0.15 mM Ca2+ labelled with carrier‐free 85Sr for 6 h (Harrison‐Murray and Clarkson, 1973). The thermodynamic and kinetic feasibility of delivering Ca2+ to the xylem exclusively through endodermal cells The scheme for Ca delivery to the xylem based on exclusive transport through endodermal cells requires the presence of sufficient plasma membrane Ca2+ channels on the cortical side and sufficient Ca2+ efflux transporters on the stelar side of the Casparian band to catalyse the observed Ca2+ flux to the xylem. There is a considerable electrochemical gradient driving Ca2+ influx through Ca2+ channels into all root cells (White, 1998; Kiegle et al., 2000b). Several types of Ca2+‐permeable channels have been recorded in the plasma membrane of root cells. These include depolarization‐activated Ca2+ channels (White, 1998, 2000), hyperpolarization‐activated Ca2+ channels (Kiegle et al., 2000a; Véry and Davies, 2000), voltage‐insensitive cation (VIC) channels (Davenport and Tester, 2000), and outward‐rectifying cation (KORC or NORC) channels (De Boer, 1999). In addition, it is likely that both mechanosensitive (stretch‐activated) and second messenger‐activated Ca2+ channels are also present (White, 1998; Leng et al., 1999). All these channels have been attributed roles in intracellular signalling. Since plasma membrane depolarization is a non‐specific response to many stimuli, depolarization‐activated Ca2+channels are thought to generate a universal signal priming plant cells for an immediate response (White, 1998). Hyperpolarization‐activated Ca2+ channels are necessary for Ca2+‐influx to (hyperpolarized) elongating root cells, such as cells in the elongation zone and root hair cells, and may determine the rate and direction of root cell elongation (Kiegle et al., 2000a; Véry and Davies, 2000). Mechanosensitive channels are thought to play a role in the regulation of turgor, and in determining the allometry of cell expansion and morphogenesis (White, 1998). The autoregulatory properties ensuing from Ca2+ influx through KORC and NORC has suggested the control of non‐specific ion efflux from root cells (De Boer, 1999). Second messenger‐activated Ca2+ channels have been implicated in defence responses and voltage‐insensitive Ca2+ channels are probably required to maintain a constant, basal [Ca2+]cyt in the resting cell (White, 1998). The possibility that any of these channels contribute to nutritional Ca fluxes has not been considered. Indeed, little is known even about their distribution within the root. However, it has been estimated that the density of Ca2+ channels in the plasma membrane of endodermal cells required to catalyse the observed Ca2+ flux to the xylem would be in excess of 2 channels μm−2 (White, 1998). This value is high, but not inconceivable. The presence of Ca2+‐ATPases in the plasma membrane of root cells has been demonstrated both biochemically (Evans and Williams, 1998; Giesler et al., 2000) and electrophysiologically (Felle et al., 1992). It is thermodynamically feasible for this transport mechanism to pump Ca2+ from the cytoplasm to the stelar apoplast. However, there is some doubt as to whether Ca2+‐ATPases could catalyse sufficient Ca2+ flux to the xylem to support the nutritional demands of the shoot (White, 1998). If the Ca2+ flux to the xylem occurred exclusively through endodermal cells, the density of Ca2+‐ATPase required would exceed the protein packing capacity of the plasma membrane. Indeed, even if many cell‐types within the stele contributed to Ca2+ efflux from the symplast to xylem, the mechanism would still be kinetically challenged. Thus, it is unlikely that a symplastic pathway alone could deliver the necessary physiological Ca2+ flux to the xylem. The observation that the Ca2+ concentration of xylem sap exuding from excised roots may exceed that of the medium bathing the roots when plants are grown in solutions containing submillimolar Ca2+ (Lazaroff and Pitman, 1966; White et al., 1992) is often cited as evidence for active Ca2+ transport to the stele. However, this phenomenon can be attributed simply to the stelar apoplast having an electrical potential more negative than the bathing medium and, thereby, concentrating cations in the xylem (Shone, 1968; De Boer, 1999). An apoplastic bypass for calcium transport to the xylem If Ca2+ reached the xylem by a symplastic pathway, its flux would be expected to show the characteristics of protein‐catalysed transport. Thus, symplastic Ca2+ transport to the xylem should be selective, there should be competition for transport between permeant cations, and the transport process should saturate at high concentrations of permeant cations. The Ca2+ channels in the plasma membrane of root cells show significant discrimination between permeant cations (White, 1998; Véry and Davies, 2000). In general, Ba2+ is more permeable than either Sr2+ or Ca2+. This is consistent with observations that the accumulation ratios for Sr/Ca and Ba/Ca in plant roots exceed those in the solution bathing the roots (Russell, 1963; Andersen, 1967; Moore et al., 1998), and that divalent cations compete for uptake into excised roots (Epstein and Leggett, 1954). Similarly, the Ca2+‐ATPases of plants, fungi and animals exhibit a high specificity for the transported cation, preferring Ca2+ to Ba2+ or Sr2+ (Liang et al., 1997; Mandal et al., 2000). For transport to the shoot, by contrast, there appears to be no selectivity between Ca2+, Ba2+ and Sr2+ (Fig. 3). Indeed, it is frequently observed that the Ca:Ba:Sr ratio in the shoot is identical to that of the solution to which roots are exposed (Collander, 1941; Menzel and Heald, 1955; Bowen and Dymond, 1956; Young and Rasmusson, 1966; Moore et al., 1998), and that there is a close correlation between the accumulation of Ca, Sr and Ba by plant species grown in the same substrate (Russell, 1963; Andersen, 1967; Wyttenbach et al., 1995; Veresoglou et al., 1996). This is found for all plant species and is not influenced by plant development. It has also been observed that the presence of Ba or Sr in an agar substrate did not affect the shoot Ca content of Arabidopsis plants, and vice versa (Fig. 3). These observations imply that there is no competition between these divalent cations for transport to the shoot, despite the fact that they compete for uptake into root cells (Epstein and Leggett, 1954). Since the cation transporters on cell membranes are selective, these observations are not consistent with the symplastic pathway through the root being an exclusive route for Ca2+, Ba2+ and Sr2+ movement to the xylem. The accumulation of Ca, Ba and Sr by shoot tissue is often linearly related to the concentrations of these cations in the nutrient solution (Fig. 3; Rediske and Selders, 1953; Russell and Squire, 1958; English and Barker, 1987). This contrasts markedly with divalent cation uptake by root cells (Epstein and Leggett, 1954), influx through Ca2+ channels (White et al., 2000) and Ca2+‐ATPase activities (Evans and Williams, 1998), which show hyperbolic relationships with increasing divalent cation concentrations. The absence of a saturable component to the transport process, which might be expected if a transport protein was involved, again suggests an apoplastic route to the xylem. Furthermore, the significant effect of transpiration on Ca2+ fluxes to the shoot (Lazeroff and Pitman, 1966; Marschner, 1995) may be taken as additional, circumstantial evidence of significant apoplastic fluxes to the xylem. Apoplastic Ca2+ would be translocated with the transpiration stream by solvent drag, and the rate at which Ca2+ is delivered to the xylem would depend on the rate of apoplastic water flow. Fig. 3. View largeDownload slide The divalent cation content of shoots of Arabidopsisthaliana (Columbia, gl1) plants grown for 21 d in 0.8% (w/v) agar containing a complete nutrient medium (based on Murashige and Skoog, 1962) with either 3 mM Ca (closed symbols) or 10 mM Ca (open symbols), and varying concentrations of Ba or Sr. Nutrient media lacked sulphate in all experiments with Ba. (A) The shoot Sr content (circles) increased linearly with increasing Sr content of the agar. Similarly, the shoot Ca content (squares) increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Sr content, and increasing the Sr content of the agar had little effect on the shoot Ca content. (B) The shoot Ba content (circles) increased linearly with increasing Ba content of the agar. The shoot Ca content (squares) similarly increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Ba content, and increasing the Ba content of the agar had little effect on the shoot Ca content. (C, D) The Ba : Ca and the Sr : Ca ratios in the shoot tissues were identical to those in the agar. Data are means from three or four experiments (HC Bowen and PJ White, unpublished data). Fig. 3. View largeDownload slide The divalent cation content of shoots of Arabidopsisthaliana (Columbia, gl1) plants grown for 21 d in 0.8% (w/v) agar containing a complete nutrient medium (based on Murashige and Skoog, 1962) with either 3 mM Ca (closed symbols) or 10 mM Ca (open symbols), and varying concentrations of Ba or Sr. Nutrient media lacked sulphate in all experiments with Ba. (A) The shoot Sr content (circles) increased linearly with increasing Sr content of the agar. Similarly, the shoot Ca content (squares) increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Sr content, and increasing the Sr content of the agar had little effect on the shoot Ca content. (B) The shoot Ba content (circles) increased linearly with increasing Ba content of the agar. The shoot Ca content (squares) similarly increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Ba content, and increasing the Ba content of the agar had little effect on the shoot Ca content. (C, D) The Ba : Ca and the Sr : Ca ratios in the shoot tissues were identical to those in the agar. Data are means from three or four experiments (HC Bowen and PJ White, unpublished data). Further discussion and perspectives The textbook scheme suggests that Ca2+ destined for the xylem must traverse the root symplast at some stage on its journey (Fig. 1). Moreover, it specifically suggests that Ca2+ travels apoplastically across the root to the Casparian band, which it then circumvents by entering the symplast of the endodermal cell through Ca2+ channels before being actively effluxed to the stele through Ca2+‐ATPases. In theory, this would allow the root to control the rate and selectivity of Ca transport to the shoot. However, several lines of evidence suggest that this scheme is incorrect. Firstly, although the pathway is thermodynamically feasible, and endodermal cells are likely to be furnished with appropriate Ca2+ transporters, there is doubt as to whether the plasma membrane of endodermal cells could physically contain sufficient Ca2+‐ATPase proteins to catalyse the observed Ca2+ flux to the xylem. Secondly, there is no selectivity, or interactions, between Ca2+, Ba2+ and Sr2+ for transport to the shoot, and the concentrations of these cations in shoot tissue are linearly related to their concentrations in the nutrient medium. This suggests that these divalent cations are unlikely to be transported across any plasma membrane (which would impart selectivity, competition and saturation phenomena) prior to their delivery to the xylem. A substantial apoplastic bypass is, therefore, indicated for the transport of Ca to the shoot. If the Casparian band is permeable to divalent cations, it is also likely to be permeable to other ions and solutes. It is unsurprising, therefore, that an apoplastic bypass for transport to the xylem has also been suggested for Na+ (Yadav et al., 1996), Cl– (Storey and Walker, 1999) and ABA (Freundl et al., 1998) based on the strong correlation between their transport and that of tracers for apoplastic solute movement. It is also indicated by root reflection coefficients (σ) for solutes less than unity. Although the endodermis is a significant barrier to solute movement (Peterson et al., 1993; Steudle et al., 1993), reflection coefficients for solute movement across roots are generally lower than those for transport across cell membranes (Steudle et al., 1987, 1993; Rüdinger et al., 1994; Frensch et al., 1996; Freundl et al., 1998). These observations prompted Steudle and co‐workers to suggest an explicit ‘composite transport’ model for solute movement to the xylem (Steudle et al., 1993; Steudle and Peterson, 1998). This model considers the root as a complex composite structure, in which parallel pathways (symplastic and apoplastic) with contrasting transport properties contribute to the total radial transport of solutes. It is consistent with low root reflection coefficients for solutes and with the greater passive permeability and lower reflection coefficients observed in root segments closest to the apex (Frensch et al., 1996). It is also consistent with the observation that increasing water flow decreases the root reflection coefficients for solutes. At rates of high transpiration, more water will move to the xylem through an apoplastic pathway (Steudle and Peterson, 1998), and this will promote apoplastic solute transport. At low transpiration rates, such as during the night or during stress conditions (drought, high salinity, nutrient deprivation) the apoplastic pathway will be less used, and transmembrane solute fluxes will dominate. Several suggestions can be made for the location of this apoplastic bypass. First, there may be a high proportion of purely apoplastic solute flux in the root apex where the endodermis has not yet developed (Steudle and Peterson, 1998). Second, there may be a significant apoplastic flux in regions where lateral roots penetrate the endodermis (Clarkson, 1993). Third, it has been speculated that the Casparian band, even though it is the major barrier to radial solute fluxes through the apoplast (Peterson et al., 1993), is not a particularly effective barrier (Steudle et al., 1993; Frensch et al., 1996; Schreiber et al., 1999). The hypothesis that Ca reaches the xylem solely by bypassing the Casparian band through the symplast of the endodermal cell rests critically on the assumption that the Casparian Band is impermeable to Ca2+. This assumption has not been verified by direct experimentation, and it has been suggested that wax‐free Casparian bands are imperfect barriers to apoplastic fluxes of water and dissolved solutes (Sanderson, 1983; Steudle et al., 1993; Steudle and Peterson, 1998; Schreiber et al., 1999). However, if the Casparian band in the State I endodermis was measurably permeable to Ca2+, and its permeability was reduced during the development of suberin lamellae (State II endodermis), then the longitudinal profile of Ca movement to the xylem could be reinterpreted as arising (at least in part) from apoplastic transport to the xylem. Such a reduction in the permeability of the Casparian band might be effected by changes in the chemical composition of its lignin, suberin or wax components during the transition to State II endodermis (Schreiber et al., 1999; Zeier et al., 1999). If this occurred, then the properties of Ca transport to the shoot (i.e. lack of selectivity, and absence of competition between cations or flux saturation) could be reconciled with the development of the endodermis. The operation of two parallel pathways for Ca movement to the xylem could imply a functional separation of symplastic and apoplastic Ca2+ fluxes within roots. Symplastic Ca2+ fluxes would be important for root nutrition and cell signalling, whilst apoplastic Ca2+ fluxes would contribute to Ca transfer to the xylem. This arrangement is consistent with the contrasting changes observed in the specific activity of Ca2+ fluxes from radiolabelled root cells to the external medium and the xylem (White et al., 1992) and compatible with reports that plants respond to environmental stresses by modifying the apoplastic barriers in roots. One of the consequences of a dominant apoplastic pathway for Ca2+ movement to the xylem would be difficulties in controlling the magnitude and selectivity of cation fluxes to the shoot. In this context, increased endodermal suberization in response to the presence of 100 μM Cd2+ or 100 mM Na+ in the solution bathing the roots can be interpreted as an acclimatory response restricting both symplastic and apoplastic movement of toxic cations to the xylem (Schrieber et al., 1999). In conclusion, there are likely to be two parallel pathways across roots delivering Ca2+to the xylem. These are considered to be (1) through the symplast of endodermal cells or (2) entirely through the apoplast. The relative magnitudes of Ca2+ fluxes through these two pathways are unknown. Although the textbook suggests that the symplastic pathway dominates, there is circumstantial evidence that apoplastic transport of Ca2+to the xylem may also occur. Indeed, utilising an apoplastic pathway for Ca2+ movement to the xylem may be a preferred option by which the root can fulfil the demand of the shoot for Ca without compromising intracellular [Ca2+]cyt signals. To understand the physiology of divalent cation relations in plants, it will be necessary to estimate the relative magnitudes of Ca2+fluxes through the symplastic and apoplastic pathways and how these are affected by developmental and environmental parameters. 1 Fax: +44 1789 470552. E‐mail: philip‐[email protected] I thank Helen Bowen, Martin Broadley, Mike Malone, Richard Napier, and Kathryn Woolaway (HRI), Ruth Rowlands and Anna Dudley (Rank Prize Funds Vacation Students), Malcolm Bennett and Sean May (Nottingham) for their contributions to the ideas presented here. I thank Marc Knight (Oxford) and Julia Davies (Cambridge) for providing unpublished manuscripts. My work is supported by the Biotechnology and Biological Sciences Research Council (UK). 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The pathways of calcium movement to the xylem

White, Philip J.
Journal of Experimental Botany , Volume 52 (358) – May 1, 2001
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0022-0957
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10.1093/jexbot/52.358.891
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Abstract

Abstract Calcium is an essential plant nutrient. It is acquired from the soil solution by the root system and translocated to the shoot via the xylem. The root must balance the delivery of calcium to the xylem with the need for individual root cells to use [Ca2+]cyt for intracellular signalling. Here the evidence for the current hypothesis, that Ca2+ travels apoplastically across the root to the Casparian band which it then circumvents via the cytoplasm of the endodermal cell, is critically reviewed. It is noted that, although Ca2+ channels and Ca2+‐ATPases are present and could catalyse Ca2+ influx and efflux across the plasma membrane of endodermal cells, their transport capacity is unlikely to be sufficient for xylem loading. Furthermore, there seems to be no competition, or interactions, between Ca2+, Ba2+ and Sr2+ for transport to the shoot. This seems incompatible with a symplastic pathway involving at least two protein‐catalysed transport steps. Thus, a quantity of purely apoplastic Ca2+ transport to the xylem is indicated. The relative contributions of these two pathways to the delivery of Ca2+ to the xylem are unknown. However, the functional separation of symplastic Ca2+fluxes (for root nutrition and cell signalling) and apoplastic Ca2+ fluxes (for transfer to the shoot) would enable the root to fulfil the demand of the shoot for calcium without compromising intracellular [Ca2+]cyt signals. This is also compatible with the observed correlation between transpiration rate and calcium delivery to the shoot. Arabidopsis thaliana, barium, calcium, Casparian band, endodermis, strontium. Introduction Calcium (Ca) is an essential plant nutrient. It fulfils a variety of structural roles, and functions as counter‐cation for inorganic and organic anions in the vacuole (Marschner, 1995). In addition, the cation (Ca2+) is essential for cell division and expansion, and explicit perturbations in cytoplasmic Ca2+ concentration ([Ca2+]cyt) link specific environmental or developmental stimuli to their appropriate physiological responses (White, 1998, 2000). Calcium is required in large amounts, and the Ca content of healthy plant tissues generally exceeds 0.1–1% dry matter. Dicotyledeonous plants require more Ca in their tissues than do monocotyledonous plants (Islam et al., 1987), which has been attributed to a larger cation exchange capacity of their cell walls (Kirkby and Pilbeam, 1984). Plants acquire Ca primarily from the soil solution through the root system, and the shoot is supplied via the xylem. In an actively growing plant the Ca flux to the xylem is high. For example, a cereal seedling with a shoot/root FW ratio of 2 and a relative growth rate of 0.2 d−1 must translocate Ca at rates approximating 40 nmol h−1 g−1 FW root to maintain its shoot Ca content at 0.1% dry weight (White, 1998). The root must balance this delivery of Ca to the xylem with the necessity for individual root cells to use [Ca2+]cyt for intracellular signalling (White, 1998; Kiegle et al., 2000b). A low (submicromolar) [Ca2+]cyt must be maintained in all root cells and [Ca2+]cyt must increase rapidly when challenged by appropriate stimuli. These properties may be compromised by high nutritional Ca2+ fluxes through root cells unless they can be controlled exquisitely. In this article the possible mechanisms by which the root might effect xylem Ca loading, without compromising cell signalling, are discussed. A particular emphasis is placed on the pathways of Ca2+ movement through the root to the xylem. Root anatomy and the structure and development of the endodermis The root is composed of many different cell types. Each cell type appears specialized to specific tasks (Clarkson, 1991; Maathuis et al., 1998). It is commonly suggested that the outer cell layers of the root, the epidermis and cortex, are involved primarily in the acquisition of water and mineral nutrients. These are separated from the cells of the stele, which are devoted to the loading, unloading and long‐distance transport of solutes in the xylem and phloem, by the endodermal cell layer (Fig. 1). The part of the root outside the plasma membrane is termed the apoplast. This includes cell walls, intercellular spaces and the lumena of tracheary elements. The interconnected cytoplasm of root cells is termed the symplast. In principle, solutes may reach the xylem either symplastically, by entering root cells and moving from cell to cell through plasmodesmata, or apoplastically, without traversing a single plasma membrane. However, in the mature root, an hydraulic separation of cortical and stelar apoplasts is imposed by the presence of an extracellular structure termed the Casparian band. This structure, which is present on the anticlinal (transverse and radial longitudinal) walls of endodermal cells, is present in all roots of vascular plants and is thought to act as a barrier to the apoplastic movement of solutes. (There appears to be a single exception to this statement. An endodermal Casparian band was not found in the roots of Lycopodium: Damus et al., 1997.) A Casparian band of some description is present throughout the root, including the regions that are considered most permeable to water and solutes, except for a few millimetres at the extreme root tip. The endodermis develops in three stages (Fig. 1; Esau, 1965; Clarkson and Robards, 1975; Peterson and Cholewa, 1998; Schreiber et al., 1999). Initially, a Casparian band is deposited within the transverse and radial longitudinal walls of the endodermal cells (State I), which becomes firmly attached to the plasma membrane of these cells. The Casparian band is composed primarily of lignin, but also contains some suberin (Schreiber et al., 1999). All cells in the endodermis develop a Casparian band approximately synchronously, following cell elongation and coincident with (or slightly prior to) the maturation of the protoxylem (Esau, 1965; Peterson and Lefcourt, 1990). At a variable distance from the apex, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II). This event frequently coincides with the emergence of lateral roots. The layers of suberin create a lamellar structure that isolates the endodermal cell protoplast from the apoplast and subsequently becomes buried by the deposition of lignified, carbohydrate cell walls (State III). These latter stages in the development of the endodermis proceed more rapidly in cells near the phloem compared to those near the xylem and ‘passage cells’, which remain in State I whilst those around them proceed to State III, can frequently be observed. It is speculated that passage cells are important in the transfer of ions to the stele in mature roots (Peterson and Enstone, 1996), because they become the only cells to expose a plasma membrane to the external solution (and therefore capable of ion uptake) when the epidermis and cortex die. The presence of suberin lamellae is thought to prevent endodermal cells from taking up solutes from the apoplast, but it is not thought to influence solute movement within the apoplast (Peterson and Cholewa, 1998). Fig. 1. View largeDownload slide Schematic views of the development of the endodermis and its hypothetical impact on the pathway of calcium movement to the xylem (Clarkson, 1993). Initially, the Casparian band develops as a modification of the anticlinal (transverse and radial longitudinal) walls between endodermal cells (State I). This is assumed to block apoplastic (cell wall) movement of calcium to the xylem, and to force the calcium destined for the xylem to enter the root symplast, through Ca2+ channels in the accessible plasma membrane of the endodermal cell. It is then assumed that this symplastic Ca2+ is pumped into the stelar apoplast by Ca2+ ATPases in the plasma membranes of cells within the stele. Subsequently, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II), and the endodermal cell becomes buried by the deposition of tertiary cell walls (State III). The deposition of suberin lamellae isolates the endodermal cell protoplast from the apoplast, preventing Ca2+ influx to endodermal cells and, thereby, calcium transport to the xylem. Fig. 1. View largeDownload slide Schematic views of the development of the endodermis and its hypothetical impact on the pathway of calcium movement to the xylem (Clarkson, 1993). Initially, the Casparian band develops as a modification of the anticlinal (transverse and radial longitudinal) walls between endodermal cells (State I). This is assumed to block apoplastic (cell wall) movement of calcium to the xylem, and to force the calcium destined for the xylem to enter the root symplast, through Ca2+ channels in the accessible plasma membrane of the endodermal cell. It is then assumed that this symplastic Ca2+ is pumped into the stelar apoplast by Ca2+ ATPases in the plasma membranes of cells within the stele. Subsequently, layers of aliphatic suberin polymers are deposited over the entire inner surface of the walls surrounding endodermal cells (State II), and the endodermal cell becomes buried by the deposition of tertiary cell walls (State III). The deposition of suberin lamellae isolates the endodermal cell protoplast from the apoplast, preventing Ca2+ influx to endodermal cells and, thereby, calcium transport to the xylem. A symplastic pathway for calcium movement to the xylem The immediate and substantial drop in root pressure upon injury of the endodermis indicates that the Casparian band is the main barrier to the radial movement of ions across the root (Peterson et al., 1993; Steudle et al., 1993). Further, it has been proposed that Ca2+cannot enter the stele via the apoplast when the Casparian band is present (Clarkson and Robards, 1975; Clarkson, 1984, 1991, 1993; Marschner, 1995). This view is based on (i) the hydrophobic chemistry of the Casparian band, (ii) the rapid penetration of divalent cations (such as Ca2+ and Sr2+) and of cell impermeant tracers (UO2+2, La3+, hydrophilic dyes) into the cortex but not the stele of plant roots and (iii) the observation that Ca2+ delivery to the xylem is increased in regions of the root where the Casparian band is discontinuous or ruptured. Calcium delivery to the xylem is maximal in the apical zone of the root (Fig. 2), which comprises both immature and recently‐matured root cells. In this region, endodermal cells possess a Casparian band (State I). Although there is no direct evidence that either lignin or suberin are effective barriers to the movement of water and dissolved solutes (Schrieber et al., 1999), it is frequently assumed that these Casparian bands are impermeable to Ca2+ and, therefore, that Ca2+ must bypass the Casparian band symplastically prior to its delivery into the xylem (Fig. 1). It is further assumed that, since Ca2+ mobility in the symplast is restricted by low [Ca2+]cyt, most radial movement of Ca across the root will occur through the apoplast up to the Casparian band. However, it should be noted that Ca2+ is only a small fraction of the total cytoplasmic Ca pool and Ca chelates might move symplastically. Since the shortest symplastic route that circumvents the Casparian band is through the cytoplasm of the endodermal cell, it is argued that Ca2+ will utilize this pathway to minimize any compromise of [Ca2+]cyt signalling mechanisms (Clarkson, 1984, 1993). Upon the deposition of suberin lamellae in the endodermis (State II and III), Ca delivery to the xylem is severely restricted, even though the endodermal cells are still symplastically connected to the cortex and stele by functional plasmodesmata. This appears to confirm the absence of a symplastic pathway for Ca movement between the cortex and stele. The observation that Ca movement to the xylem decreases as endodermal cells become inaccessible from the apoplast is held to support the view that Ca destined for the xylem enters the symplast exclusively through endodermal cells. In basal regions of the root some Ca may reach the xylem through the apoplast as lateral roots emerge. During lateral root formation, the endodermal cells divide and the newly formed radial walls lack a Casparian band (Peterson and Lefcourt, 1990). However, Casparian bands are deposited at the base of lateral root primordia and rapidly become continuous with those of the endodermis of the parent root. Similarly, although the endodermal Casparian band may lose its function as an apoplastic barrier when roots undergo secondary (thickening) growth, this occurs only after it is replaced by the periderm (Esau, 1965; Weerdenburg and Peterson, 1984). In the roots of many plant species, particularly when grown in soil, an exodermis (hypodermis) develops that has both Casparian bands and suberin lamellae with chemical compositions and properties similar to those of the endodermis (Perumalla et al., 1990; Peterson and Perumalla, 1990; Damus et al., 1997; Schreiber et al., 1999). However, the integrity of the exodermal Casparian band is disrupted by the emergence of lateral roots, and its development is patchy, absolutely dependent upon environmental conditions (it does not form readily in plants grown hydroponically) and frequently subsequent to the suberization of the endodermis (Enstone and Peterson, 1992, 1997, 1998). Thus, in most cases, a complete Casparian band in the exodermis will be limited to regions where Ca delivery to the xylem would be minimal even in its absence, and so this structure is unlikely to influence Ca movement to the xylem. Consistent with this view, Zimmermann and Steudle (1998) observed that the transport to the xylem of the apoplastic dye PTS (trisodium 3‐hydroxy‐5,8,10‐pyrene‐trisulphonate) was not affected by the presence of an exodermal Casparian band. A scheme for Ca delivery to the xylem based on exclusive Ca2+ transport through endodermal cells is found in many textbooks (Clarkson, 1991; Marschner, 1995). In this scheme, Ca2+ is considered to travel apoplastically across the root to the Casparian band. To circumvent the Casparian band, it is proposed that Ca2+ enters the cytoplasm of the endodermal cell through Ca2+‐permeable channels. It is then actively effluxed from the symplast by the plasma membrane Ca2+‐ATPases or Ca2+/H+ antiporters of cells within the stele. In theory, the necessity for Ca2+ to traverse the plasma membrane of endodermal cells would allow the root to control the rate and selectivity of Ca transport to the shoot. The selectivity of the apoplastic route, which is determined by the ion exchange properties of the cell wall, is minimal. However, by diverting the cation flow through the cell, transport proteins in the cell membranes can selectively catalyse the movement of Ca2+ to the xylem (Clarkson, 1991). This could benefit the plant by restricting the movement of toxic cations to the shoot. However, several lines of evidence suggest that this simple scheme might be incorrect. In the next section the thermodynamic and kinetic feasibility of the symplastic transport pathway will be assessed. Then the apparent absence of selectivity or competition between divalent cations for transport to the shoot (both of which are characteristics of protein‐mediated transport pathways) will be considered. Fig. 2. View largeDownload slide The profile of calcium translocation to the shoot along the seminal root of marrow (Cucurbita pepo L.), and its relationship with the development of the endodermis. Calcium translocation is maximal in the root apical zone, where the endodermal cells possess a Casparian band (State I endodermis) and xylem vessels first become fully conductive, and declines as the endodermal cells become increasingly suberised (State II endodermis). Results were obtained by enclosing short (3.5 mm) sections of seminal roots in flow cells containing 0.15 mM Ca2+ labelled with carrier‐free 85Sr for 6 h (Harrison‐Murray and Clarkson, 1973). Fig. 2. View largeDownload slide The profile of calcium translocation to the shoot along the seminal root of marrow (Cucurbita pepo L.), and its relationship with the development of the endodermis. Calcium translocation is maximal in the root apical zone, where the endodermal cells possess a Casparian band (State I endodermis) and xylem vessels first become fully conductive, and declines as the endodermal cells become increasingly suberised (State II endodermis). Results were obtained by enclosing short (3.5 mm) sections of seminal roots in flow cells containing 0.15 mM Ca2+ labelled with carrier‐free 85Sr for 6 h (Harrison‐Murray and Clarkson, 1973). The thermodynamic and kinetic feasibility of delivering Ca2+ to the xylem exclusively through endodermal cells The scheme for Ca delivery to the xylem based on exclusive transport through endodermal cells requires the presence of sufficient plasma membrane Ca2+ channels on the cortical side and sufficient Ca2+ efflux transporters on the stelar side of the Casparian band to catalyse the observed Ca2+ flux to the xylem. There is a considerable electrochemical gradient driving Ca2+ influx through Ca2+ channels into all root cells (White, 1998; Kiegle et al., 2000b). Several types of Ca2+‐permeable channels have been recorded in the plasma membrane of root cells. These include depolarization‐activated Ca2+ channels (White, 1998, 2000), hyperpolarization‐activated Ca2+ channels (Kiegle et al., 2000a; Véry and Davies, 2000), voltage‐insensitive cation (VIC) channels (Davenport and Tester, 2000), and outward‐rectifying cation (KORC or NORC) channels (De Boer, 1999). In addition, it is likely that both mechanosensitive (stretch‐activated) and second messenger‐activated Ca2+ channels are also present (White, 1998; Leng et al., 1999). All these channels have been attributed roles in intracellular signalling. Since plasma membrane depolarization is a non‐specific response to many stimuli, depolarization‐activated Ca2+channels are thought to generate a universal signal priming plant cells for an immediate response (White, 1998). Hyperpolarization‐activated Ca2+ channels are necessary for Ca2+‐influx to (hyperpolarized) elongating root cells, such as cells in the elongation zone and root hair cells, and may determine the rate and direction of root cell elongation (Kiegle et al., 2000a; Véry and Davies, 2000). Mechanosensitive channels are thought to play a role in the regulation of turgor, and in determining the allometry of cell expansion and morphogenesis (White, 1998). The autoregulatory properties ensuing from Ca2+ influx through KORC and NORC has suggested the control of non‐specific ion efflux from root cells (De Boer, 1999). Second messenger‐activated Ca2+ channels have been implicated in defence responses and voltage‐insensitive Ca2+ channels are probably required to maintain a constant, basal [Ca2+]cyt in the resting cell (White, 1998). The possibility that any of these channels contribute to nutritional Ca fluxes has not been considered. Indeed, little is known even about their distribution within the root. However, it has been estimated that the density of Ca2+ channels in the plasma membrane of endodermal cells required to catalyse the observed Ca2+ flux to the xylem would be in excess of 2 channels μm−2 (White, 1998). This value is high, but not inconceivable. The presence of Ca2+‐ATPases in the plasma membrane of root cells has been demonstrated both biochemically (Evans and Williams, 1998; Giesler et al., 2000) and electrophysiologically (Felle et al., 1992). It is thermodynamically feasible for this transport mechanism to pump Ca2+ from the cytoplasm to the stelar apoplast. However, there is some doubt as to whether Ca2+‐ATPases could catalyse sufficient Ca2+ flux to the xylem to support the nutritional demands of the shoot (White, 1998). If the Ca2+ flux to the xylem occurred exclusively through endodermal cells, the density of Ca2+‐ATPase required would exceed the protein packing capacity of the plasma membrane. Indeed, even if many cell‐types within the stele contributed to Ca2+ efflux from the symplast to xylem, the mechanism would still be kinetically challenged. Thus, it is unlikely that a symplastic pathway alone could deliver the necessary physiological Ca2+ flux to the xylem. The observation that the Ca2+ concentration of xylem sap exuding from excised roots may exceed that of the medium bathing the roots when plants are grown in solutions containing submillimolar Ca2+ (Lazaroff and Pitman, 1966; White et al., 1992) is often cited as evidence for active Ca2+ transport to the stele. However, this phenomenon can be attributed simply to the stelar apoplast having an electrical potential more negative than the bathing medium and, thereby, concentrating cations in the xylem (Shone, 1968; De Boer, 1999). An apoplastic bypass for calcium transport to the xylem If Ca2+ reached the xylem by a symplastic pathway, its flux would be expected to show the characteristics of protein‐catalysed transport. Thus, symplastic Ca2+ transport to the xylem should be selective, there should be competition for transport between permeant cations, and the transport process should saturate at high concentrations of permeant cations. The Ca2+ channels in the plasma membrane of root cells show significant discrimination between permeant cations (White, 1998; Véry and Davies, 2000). In general, Ba2+ is more permeable than either Sr2+ or Ca2+. This is consistent with observations that the accumulation ratios for Sr/Ca and Ba/Ca in plant roots exceed those in the solution bathing the roots (Russell, 1963; Andersen, 1967; Moore et al., 1998), and that divalent cations compete for uptake into excised roots (Epstein and Leggett, 1954). Similarly, the Ca2+‐ATPases of plants, fungi and animals exhibit a high specificity for the transported cation, preferring Ca2+ to Ba2+ or Sr2+ (Liang et al., 1997; Mandal et al., 2000). For transport to the shoot, by contrast, there appears to be no selectivity between Ca2+, Ba2+ and Sr2+ (Fig. 3). Indeed, it is frequently observed that the Ca:Ba:Sr ratio in the shoot is identical to that of the solution to which roots are exposed (Collander, 1941; Menzel and Heald, 1955; Bowen and Dymond, 1956; Young and Rasmusson, 1966; Moore et al., 1998), and that there is a close correlation between the accumulation of Ca, Sr and Ba by plant species grown in the same substrate (Russell, 1963; Andersen, 1967; Wyttenbach et al., 1995; Veresoglou et al., 1996). This is found for all plant species and is not influenced by plant development. It has also been observed that the presence of Ba or Sr in an agar substrate did not affect the shoot Ca content of Arabidopsis plants, and vice versa (Fig. 3). These observations imply that there is no competition between these divalent cations for transport to the shoot, despite the fact that they compete for uptake into root cells (Epstein and Leggett, 1954). Since the cation transporters on cell membranes are selective, these observations are not consistent with the symplastic pathway through the root being an exclusive route for Ca2+, Ba2+ and Sr2+ movement to the xylem. The accumulation of Ca, Ba and Sr by shoot tissue is often linearly related to the concentrations of these cations in the nutrient solution (Fig. 3; Rediske and Selders, 1953; Russell and Squire, 1958; English and Barker, 1987). This contrasts markedly with divalent cation uptake by root cells (Epstein and Leggett, 1954), influx through Ca2+ channels (White et al., 2000) and Ca2+‐ATPase activities (Evans and Williams, 1998), which show hyperbolic relationships with increasing divalent cation concentrations. The absence of a saturable component to the transport process, which might be expected if a transport protein was involved, again suggests an apoplastic route to the xylem. Furthermore, the significant effect of transpiration on Ca2+ fluxes to the shoot (Lazeroff and Pitman, 1966; Marschner, 1995) may be taken as additional, circumstantial evidence of significant apoplastic fluxes to the xylem. Apoplastic Ca2+ would be translocated with the transpiration stream by solvent drag, and the rate at which Ca2+ is delivered to the xylem would depend on the rate of apoplastic water flow. Fig. 3. View largeDownload slide The divalent cation content of shoots of Arabidopsisthaliana (Columbia, gl1) plants grown for 21 d in 0.8% (w/v) agar containing a complete nutrient medium (based on Murashige and Skoog, 1962) with either 3 mM Ca (closed symbols) or 10 mM Ca (open symbols), and varying concentrations of Ba or Sr. Nutrient media lacked sulphate in all experiments with Ba. (A) The shoot Sr content (circles) increased linearly with increasing Sr content of the agar. Similarly, the shoot Ca content (squares) increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Sr content, and increasing the Sr content of the agar had little effect on the shoot Ca content. (B) The shoot Ba content (circles) increased linearly with increasing Ba content of the agar. The shoot Ca content (squares) similarly increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Ba content, and increasing the Ba content of the agar had little effect on the shoot Ca content. (C, D) The Ba : Ca and the Sr : Ca ratios in the shoot tissues were identical to those in the agar. Data are means from three or four experiments (HC Bowen and PJ White, unpublished data). Fig. 3. View largeDownload slide The divalent cation content of shoots of Arabidopsisthaliana (Columbia, gl1) plants grown for 21 d in 0.8% (w/v) agar containing a complete nutrient medium (based on Murashige and Skoog, 1962) with either 3 mM Ca (closed symbols) or 10 mM Ca (open symbols), and varying concentrations of Ba or Sr. Nutrient media lacked sulphate in all experiments with Ba. (A) The shoot Sr content (circles) increased linearly with increasing Sr content of the agar. Similarly, the shoot Ca content (squares) increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Sr content, and increasing the Sr content of the agar had little effect on the shoot Ca content. (B) The shoot Ba content (circles) increased linearly with increasing Ba content of the agar. The shoot Ca content (squares) similarly increased with increasing Ca content of the agar. The Ca content of the agar had no effect on shoot Ba content, and increasing the Ba content of the agar had little effect on the shoot Ca content. (C, D) The Ba : Ca and the Sr : Ca ratios in the shoot tissues were identical to those in the agar. Data are means from three or four experiments (HC Bowen and PJ White, unpublished data). Further discussion and perspectives The textbook scheme suggests that Ca2+ destined for the xylem must traverse the root symplast at some stage on its journey (Fig. 1). Moreover, it specifically suggests that Ca2+ travels apoplastically across the root to the Casparian band, which it then circumvents by entering the symplast of the endodermal cell through Ca2+ channels before being actively effluxed to the stele through Ca2+‐ATPases. In theory, this would allow the root to control the rate and selectivity of Ca transport to the shoot. However, several lines of evidence suggest that this scheme is incorrect. Firstly, although the pathway is thermodynamically feasible, and endodermal cells are likely to be furnished with appropriate Ca2+ transporters, there is doubt as to whether the plasma membrane of endodermal cells could physically contain sufficient Ca2+‐ATPase proteins to catalyse the observed Ca2+ flux to the xylem. Secondly, there is no selectivity, or interactions, between Ca2+, Ba2+ and Sr2+ for transport to the shoot, and the concentrations of these cations in shoot tissue are linearly related to their concentrations in the nutrient medium. This suggests that these divalent cations are unlikely to be transported across any plasma membrane (which would impart selectivity, competition and saturation phenomena) prior to their delivery to the xylem. A substantial apoplastic bypass is, therefore, indicated for the transport of Ca to the shoot. If the Casparian band is permeable to divalent cations, it is also likely to be permeable to other ions and solutes. It is unsurprising, therefore, that an apoplastic bypass for transport to the xylem has also been suggested for Na+ (Yadav et al., 1996), Cl– (Storey and Walker, 1999) and ABA (Freundl et al., 1998) based on the strong correlation between their transport and that of tracers for apoplastic solute movement. It is also indicated by root reflection coefficients (σ) for solutes less than unity. Although the endodermis is a significant barrier to solute movement (Peterson et al., 1993; Steudle et al., 1993), reflection coefficients for solute movement across roots are generally lower than those for transport across cell membranes (Steudle et al., 1987, 1993; Rüdinger et al., 1994; Frensch et al., 1996; Freundl et al., 1998). These observations prompted Steudle and co‐workers to suggest an explicit ‘composite transport’ model for solute movement to the xylem (Steudle et al., 1993; Steudle and Peterson, 1998). This model considers the root as a complex composite structure, in which parallel pathways (symplastic and apoplastic) with contrasting transport properties contribute to the total radial transport of solutes. It is consistent with low root reflection coefficients for solutes and with the greater passive permeability and lower reflection coefficients observed in root segments closest to the apex (Frensch et al., 1996). It is also consistent with the observation that increasing water flow decreases the root reflection coefficients for solutes. At rates of high transpiration, more water will move to the xylem through an apoplastic pathway (Steudle and Peterson, 1998), and this will promote apoplastic solute transport. At low transpiration rates, such as during the night or during stress conditions (drought, high salinity, nutrient deprivation) the apoplastic pathway will be less used, and transmembrane solute fluxes will dominate. Several suggestions can be made for the location of this apoplastic bypass. First, there may be a high proportion of purely apoplastic solute flux in the root apex where the endodermis has not yet developed (Steudle and Peterson, 1998). Second, there may be a significant apoplastic flux in regions where lateral roots penetrate the endodermis (Clarkson, 1993). Third, it has been speculated that the Casparian band, even though it is the major barrier to radial solute fluxes through the apoplast (Peterson et al., 1993), is not a particularly effective barrier (Steudle et al., 1993; Frensch et al., 1996; Schreiber et al., 1999). The hypothesis that Ca reaches the xylem solely by bypassing the Casparian band through the symplast of the endodermal cell rests critically on the assumption that the Casparian Band is impermeable to Ca2+. This assumption has not been verified by direct experimentation, and it has been suggested that wax‐free Casparian bands are imperfect barriers to apoplastic fluxes of water and dissolved solutes (Sanderson, 1983; Steudle et al., 1993; Steudle and Peterson, 1998; Schreiber et al., 1999). However, if the Casparian band in the State I endodermis was measurably permeable to Ca2+, and its permeability was reduced during the development of suberin lamellae (State II endodermis), then the longitudinal profile of Ca movement to the xylem could be reinterpreted as arising (at least in part) from apoplastic transport to the xylem. Such a reduction in the permeability of the Casparian band might be effected by changes in the chemical composition of its lignin, suberin or wax components during the transition to State II endodermis (Schreiber et al., 1999; Zeier et al., 1999). If this occurred, then the properties of Ca transport to the shoot (i.e. lack of selectivity, and absence of competition between cations or flux saturation) could be reconciled with the development of the endodermis. The operation of two parallel pathways for Ca movement to the xylem could imply a functional separation of symplastic and apoplastic Ca2+ fluxes within roots. Symplastic Ca2+ fluxes would be important for root nutrition and cell signalling, whilst apoplastic Ca2+ fluxes would contribute to Ca transfer to the xylem. This arrangement is consistent with the contrasting changes observed in the specific activity of Ca2+ fluxes from radiolabelled root cells to the external medium and the xylem (White et al., 1992) and compatible with reports that plants respond to environmental stresses by modifying the apoplastic barriers in roots. One of the consequences of a dominant apoplastic pathway for Ca2+ movement to the xylem would be difficulties in controlling the magnitude and selectivity of cation fluxes to the shoot. In this context, increased endodermal suberization in response to the presence of 100 μM Cd2+ or 100 mM Na+ in the solution bathing the roots can be interpreted as an acclimatory response restricting both symplastic and apoplastic movement of toxic cations to the xylem (Schrieber et al., 1999). In conclusion, there are likely to be two parallel pathways across roots delivering Ca2+to the xylem. These are considered to be (1) through the symplast of endodermal cells or (2) entirely through the apoplast. The relative magnitudes of Ca2+ fluxes through these two pathways are unknown. Although the textbook suggests that the symplastic pathway dominates, there is circumstantial evidence that apoplastic transport of Ca2+to the xylem may also occur. Indeed, utilising an apoplastic pathway for Ca2+ movement to the xylem may be a preferred option by which the root can fulfil the demand of the shoot for Ca without compromising intracellular [Ca2+]cyt signals. To understand the physiology of divalent cation relations in plants, it will be necessary to estimate the relative magnitudes of Ca2+fluxes through the symplastic and apoplastic pathways and how these are affected by developmental and environmental parameters. 1 Fax: +44 1789 470552. E‐mail: philip‐[email protected] I thank Helen Bowen, Martin Broadley, Mike Malone, Richard Napier, and Kathryn Woolaway (HRI), Ruth Rowlands and Anna Dudley (Rank Prize Funds Vacation Students), Malcolm Bennett and Sean May (Nottingham) for their contributions to the ideas presented here. I thank Marc Knight (Oxford) and Julia Davies (Cambridge) for providing unpublished manuscripts. My work is supported by the Biotechnology and Biological Sciences Research Council (UK). 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Published: May 1, 2001

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