JXB Advance Access originally published online on June 1, 2007
Journal of Experimental Botany 2007 58(10):2609-2615; doi:10.1093/jxb/erm105
RESEARCH PAPER |
Ion-mediated enhancement of xylem hydraulic conductivity is not always suppressed by the presence of Ca2+ in the sap
1Dipartimento di Biologia, Università di Trieste, Via L. Giorgieri 10, I-34127 Trieste, Italia
2Dipartimento di Scienze Botaniche, Università di Messina, Salita Sperone 31, I-98166 Messina S. Agata, Italia
* To whom correspondence should be addressed. E-mail: nardini{at}units.it
Received 22 February 2007; Revised 5 April 2007 Accepted 17 April 2007
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Abstract |
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The physiological significance of ion-mediated enhancement of xylem hydraulic conductivity (Kh) in planta has recently been questioned. The phenomenon has been suggested to be an artefact caused by the use of deionized water as a reference fluid during measurements of the impact of different ions on Kh. In the present study, ion-mediated changes in Kh were measured in twigs of five woody species during perfusion with 25 mM KCl compared with different reference fluids like deionized water, a commercial mineral water containing different ions (including 0.5 mM Ca2+), and a 1 mM CaCl2 solution. Both fully hydrated twigs and twigs with about 50% loss of hydraulic conductivity due to cavitation-induced embolism were tested. Adding 25 mM KCl to the three reference fluids caused Kh to increase by about 20%. The KCl-mediated increase of Kh was even larger (up to 100%) in embolized twigs. The presence of Ca2+ in the reference solution decreased, but not suppressed, the KCl-mediated enhancement of Kh in fully hydrated twigs of three species, but not in the other two species tested. Ca2+ did not affect the Kh response to KCl in embolized twigs. These data suggest that the recently reported suppression of the ‘ionic effect’ by the presence of calcium in the xylem sap is not a general phenomenon and that ion-mediated changes of Kh may play a role in planta partially to compensate for cavitation-induced loss of xylem hydraulic conductivity.
Key words: Calcium, hydraulic conductivity, ionic effect, pectins, sap, xylem
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Introduction |
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Long-distance water transport in vascular plants relies on the xylem, a highly efficient pipeline connecting roots to the sites of water evaporation at the leaf level (Tyree and Zimmermann, 2002; Sperry, 2003). Sufficient water flow rates must be maintained to compensate for water loss during transpiration and to prevent leaf desiccation. Moreover, gas exchange rates and, hence, photosynthesis and plant productivity largely depend on whole-plant hydraulic conductance (Sperry, 2000; Meinzer, 2002; Tyree, 2003).
Short-term changes of xylem hydraulic conductance (Kh) are a common consequence of stress-induced xylem cavitation and embolism eventually followed by xylem refilling (Améglio et al., 2002; Bucci et al., 2003; Salleo et al., 2004). In recent years, the hypothesis has been advanced that changes in the ionic concentration of xylem sap might also be responsible for short-term modulation of xylem hydraulic conductance (Zwieniecki et al., 2001). The influence of ionic solutes on xylem hydraulics was originally described by Zimmermann (1978) who observed that the use of deionized water during experiments to determine the hydraulic properties of stem segments significantly decreased Kh compared with values obtained with dilute salt solutions. More recently, Van Ieperen et al. (2000) have confirmed Zimmermann's observations and showed that solute-mediated changes in Kh were not caused by changes in the osmotic potential of the perfused solution but by the presence of cations in the fluid used during Kh measurements. This finding has been confirmed by Zwieniecki et al. (2001) and Boyce et al. (2004) in a wide range of genera and species. Furthermore, it has been suggested that the ion-mediated flow enhancement could be attributed to the shrinking of the pit membrane hydrogels (pectins) in response to the increased ionic strength of the solution perfused (Ryden et al., 2000).
Consistent with the interpretation of pit membranes as the structures responsible for ion-mediated changes in Kh, no ‘ionic effect’ was found to exist in the case of single vessels open at both sides, whilst flow between adjacent vessels or vascular bundles resulted in a strong response to 100 mM KCl (Zwieniecki et al., 2001, 2003). Gascò et al. (2006) have provided further experimental evidence for the role of pit membranes in the ‘ionic effect’, in that the ion-mediated flow enhancement increased with the stem length in agreement with the assumption that in one species the number of pits that have to be crossed by the flowing solution increases with the sample length (Sperry et al., 2005). In the same study, the ‘ionic effect’ was also reported to increase exponentially with the amount of xylem embolism induced in the stem samples. This, was interpreted to be a consequence of ionic solutions being forced to cross increasing numbers of interconduit pits to by-pass embolized conduits (Gascò et al., 2006). On the basis of this last finding, Gascò and co-workers have suggested that the ion-mediated increase of Kh might act in planta as a mechanism compensating for cavitation-induced loss of Kh. In fact, cavitation-induced enrichment of xylem sap with inorganic solutes has been described to occur in laurel twigs by Tyree et al. (1999). Further evidence for a possible role of ion-mediated regulation of xylem hydraulics in planta has recently been provided by Zwieniecki et al. (2004), showing that active exchange of solutes from phloem to xylem (De Boer and Volkov, 2003) might play a role in the regulation of water flow through the plant.
In all the above cited studies, the ion-mediated changes of Kh were quantified using KCl solutions at concentrations ranging between 0.01 mM to 100 mM which were commonly perfused after flushing twigs with deionized water as a reference fluid. Deionized water, however, is a very artificial medium and is by no means representative of xylem sap. Even at high transpiration rates, xylem sap usually contains small amounts of different ions including potassium, calcium, and magnesium among the principal cations (Herdel et al., 2001; Siebrecht et al., 2003; Goodger et al., 2005).
In a recent paper, Van Ieperen and Van Gelder (2006) have reported the suppression of ion-mediated flow changes in Chrysanthemum sp. and Prunus laurocerasus L. whenever solutions containing even small amounts of calcium (1 mM) were used as a reference fluid instead of deionized water. On the basis of these data, the authors concluded that complete removal of cations from the xylem fluid during perfusion with deionized water would contribute by over 95% to the measured ion-mediated flow changes. If this were the case, all the proposed relationships between the ionic concentration of xylem sap and changes in the water flow through the xylem should be revisited. Moreover, the results by Van Ieperen and Van Gelder (2006) pose serious doubts about the possibility that any ion-mediated effect actually occurs in planta.
In the present study, measurements of ion-mediated flow changes are reported in both fully hydrated and partially embolized twigs of five woody species. Measurements were performed using different solutions as reference fluids containing or not small amounts of calcium and other ions and comparing stem Kh to that measured using the same solutions with KCl added. Embolized twigs were included in the study with the aim of maximizing the ionic effect and, therefore, to check the eventual Ca2+-induced suppression of KCl-induced enhancement of Kh better. The rationale of this study was to assess whether the reported Ca2+-induced suppression of the ion-mediated Kh enhancement is a general phenomenon and whether alternative explanations for the phenomenon are plausible.
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Materials and methods |
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All the experiments were conducted between September and December 2006 on current-year twigs from over 20-year-old plants of Laurus nobilis L. (laurel, Lauraceae), Prunus laurocerasus L. (cherry laurel, Rosaceae), Phytolacca dioica L. (ombu, Phytolaccaceae), Ceratonia siliqua L. (carob, Fabaceae), and Persea gratissima L. (avocado, Lauraceae). Trees of L. nobilis and P. laurocerasus were growing in the Botanical Garden of the Department of Biology, University of Trieste (North-Eastern Italy), while the other three species were growing in the Botanical Garden of the University of Messina (Sicily). Stem segments were cut off from the middle part of twigs 20–50 cm long. Samples were obtained from stems 5–7 mm thick (basal diameter). Preferred sample lengths were 16 cm for Pe. gratissima, 12 cm for L. nobilis and C. siliqua, 11 cm for Ph. dioica, and 6 cm for Pr. laurocerasus. These sample lengths were selected on the basis of preliminary measurements of the vessel length distribution (Gascò et al., 2006) showing that the largest fraction of vessels (65–95%) were shorter than the above sample lengths. Twigs were cut off in the field under distilled water to prevent embolism and transported within 5 min to the laboratory where they were connected to the apparatus for hydraulic measurements. The instrument used to this purpose was the XYL'EM (Xylem Embolism Meter, Bronkhorst, Montigny les Cormeilles, France), which is based on a high-resolution liquid mass flowmeter (for details about the instrument, see Cochard et al., 2000).
Native calcium concentration in the xylem sap of laurel
Current-year twigs from L. nobilis plants were cut off in the field under distilled water in the morning (08.00 h to 09.00 h) and immediately transported to the laboratory. About 3 mm of their distal cut end was girdled (i.e. the bark was removed) to prevent any contamination of xylem sap with phloem exudate. Twigs were then connected to the hydraulic apparatus at their proximal end and perfused at P=9 kPa with deionized water filtered to 0.1 µm. Two serial sap samples of 10–12 µl were collected after 2 min and 5 min. In fact, preliminary experiments had shown that the osmolarity of sap samples (as measured using a micro-osmometer, model 110, Fiske Associated, Norwood, MA, USA) was approximately constant at 20 mOsm kg–1 during the first 10 min and then declined progressively to zero as deionized water began to mix with natural xylem sap. Hence, the ion content of samples collected within the first 5 min could safely be taken as ‘native’ ionic composition of xylem sap. K+, Na+, Ca2+, and Mg2+ contents were measured using an atomic absorption spectrometer (model 5000, Perkin-Elmer). Measurements were repeated on five different twigs and ion content was calculated for each twig as the mean of samples collected 2 min and 5 min after starting perfusion. The ion content of xylem sap of the other four species was not measured.
Hydraulic measurements
The species under study were measured for the ion-mediated enhancement of Kh during perfusion of twigs with 25 mM KCl solutions that were prepared using three different fluids, namely deionized water, a commercial mineral water containing 0.5 mM Ca2+ (only in the case of L. nobilis), and a 1 mM CaCl2 solution. The same fluids without KCl were used as reference fluids. Potassium chloride was used to assess the ion-mediated effect on Kh because K+ is the most abundant cation in the xylem sap and represents about 50% of total inorganic ion concentration (Siebrecht et al., 2003). Moreover, a previous study by Tyree et al. (1999) had reported xylem sap osmolarities of L. nobilis twigs to be up to 50 mOsm kg–1 following pressure-induced xylem cavitation, which would correspond to a [KCl] of 25 mM. The mineral water used during experiments (Levissima, San Pellegrino SpA, Milano, Italy), contained several different ions including Ca2+ at a concentration of 0.51 mM (Table 1) and was intended to simulate better the xylem sap ionic content with respect to fluids containing only one cation (K+ or Ca2+). The pH of the solutions tested was 6.6 in the case of deionized water and CaCl2 solution and 7.4 in the case of the commercial mineral water as measured using a pH-meter (Twin mod. B-213, Horiba Ltd., Kyoto, Japan). All the perfused fluids were filtered to 0.1 µm to prevent conduit clogging due to suspended particles and debris.
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Twigs were first measured for Kh using one of the three selected reference fluids (see above). Samples were initially flushed at a pressure (P) of 0.19 MPa for 10 min to remove native emboli and then measured for Kh at P=9 kPa until the flow became stable which took about 30 min. The same reference solution added with 25 mM KCl was tested and the relative increase of Kh was recorded (
Kh). All hydraulic measurements were conducted in a laboratory maintained at constant temperature and corrected for viscosity at 20 °C. At least five twigs per species were used for each reference fluid tested.
A second group of samples consisted of twigs where xylem embolism had been induced during bench dehydration. To prevent too rapid stem dehydration, three-year-old branches were cut off and left dehydrating for about 1 h. Single twigs to be tested for Kh were cut off from branches. The percentage loss of hydraulic conductivity (PLC) was measured using the method described in detail by Salleo et al. (1996, 2004). PLC measurements were performed in the course of each experiment (see below) and only data from twigs with a PLC of about 50% were analysed further. Air-dehydrated stems were cut into segments of the desired length and perfused with one of the three reference fluids (see above) at P=9 kPa until the flow became constant to get the initial Kh (Kh–i). The same reference fluid added with KCl to get 25 mM KCl concentration was then injected into the samples at the same pressure, thus getting the new initial Kh. Samples were then flushed with the reference solution (without KCl) at P=0.19 MPa for 10 min to remove emboli (thus getting Kh–max) and re-measured for Kh at low pressure (P=9 kPa), again with the pure reference solution. This procedure allowed us to get the Kh induced by 25 mM KCl in embolized stem segments compared with the Kh measured with different reference fluids. The percentage loss of hydraulic conductivity (PLC) of stem samples was computed as (1–Kh–i/Kh–max)x100.
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Experiments on L. nobilis
The xylem sap collected from fully hydrated laurel twigs was revealed to have a native Ca2+ concentration of about 1 mM (Table 2). Significant amounts of Mg2+ (about 0.5 mM) as well as of K+ and Na+ (about 3 mM) were also detected. Therefore, Ca2+ concentrations used in our reference fluids were well within native Ca2+ concentrations measured in xylem sap of L. nobilis twigs. In turn, the commercial mineral water tested as reference solution (Table 1) roughly matched the natural composition of a dilute xylem sap (Siebrecht et al., 2003).
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Laurel twigs showed a
Kh of the order of +17% to +20% in response to adding 25 mM KCl to the reference fluid, i.e. the measured Kh was comparable to that reported by Gascò et al. (2006) for the same species. No statistically significant difference in Kh was found to exist among samples perfused with the different reference fluids, i.e. deionized water, mineral water containing 0.5 mM Ca2+, and 1 mM CaCl2 solution (Fig. 1A). Air-dehydrated laurel twigs underwent PLC of 52±7%. In the presence of this amount of embolism, 25 mM KCl caused a Kh increase of about 60–70% compared with Kh measured with reference fluids. Again, no statistically significant difference in Kh was recorded among embolized samples, regardless of whether it was initially perfused with deionized water or multi-ionic solution or 1 mM CaCl2 solution (Fig. 1B).
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Experiments on Pr. laurocerasus, Ph. dioica, C. siliqua, and Pe. gratissima
Fully hydrated twigs of the species studied showed 10–22% increase in Kh when 25 mM KCl was added to deionized water (Fig. 2A). The ion-mediated flow enhancement was strongly reduced in Pr. laurocerasus, Ph. dioica, and C. siliqua when 1 mM Ca2+ was present in the reference solution. In particular, Ca2+ decreased the K+-induced
Kh by about 60% in these three species. By contrast, no effect of Ca2+ was recorded for twigs of Pe. gratissima which behaved similarly to L. nobilis twigs (Fig. 2A).
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Twigs dehydrated to a PLC of about 50% showed
Kh of +60% to +100% when 25 mM KCl was added to deionized water. Such a Kh enhancement effect was not reduced by 1 mM CaCl2 when present in the reference solution (Fig. 2B). |
Discussion |
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Our data indicate that significant enhancement of Kh occurred in response to K+ in all the species studied. Also, this ionic effect was strongly amplified in embolized samples compared with fully hydrated ones in the five species tested. The presence of Ca2+ ions in the reference fluid did not alter the ‘ionic effect’ in two out of five species (L. nobilis and Pe. gratissima). In the other three species, the reference solution containing 1 mM CaCl2 reduced the Kh increase by about 60% compared to values obtained using deionized water as a reference fluid.
Van Ieperen and Van Gelder (2006) have reported an almost complete suppression (a 95% reduction) in the ion-mediated increase of Kh in Pr. laurocerasus twigs when 1 mM CaCl2 was used as a reference fluid. They interpreted this result as evidence that the small amount of cations usually present in the xylem sap would be sufficient to maximize the electrostatic screening of the de-esterified groups in the pectin matrix of pit membranes and, hence, minimize pectin gel volume and xylem hydraulic resistance. These authors further suggested that a high K+/Ca2+ ratio in the solution flowing through the xylem conduits would cause a measurable loss of Ca2+ from the pectin matrix, therefore inducing a possible loss of the degree of crosslinking of the pectin chains, reduced rigidity and, hence, larger swelling of the pectin matrix. When K+-containing solutions were injected after deionized water, they would strongly but artefactually amplify the ‘ionic effect’.
A generally accepted primary structure of pectins has emerged from a huge number of studies spanning the last decades (see Ridley et al., 2001, for a review on the topic). The results of these studies, when taken together, lead to the general conclusion that pectic components can crosslink in several ways. In particular, homogalacturonan (HG) chains can crosslink through Ca2+ bridges or enclosing Ca2+ ions (the ‘egg box’ model). In both cases, the ion exchange isotherms show a strong affinity of HG for Ca2+ over other monovalent ions like K+. The affinity of HG for Ca2+ is believed to increase with the average degree of methyl esterification (DE) (Tibbits et al., 1998; Ridley et al., 2001). Removal of Ca2+ from HG can readily occur depending on several physical variables such as the cation exchange capacity, the type of pectins, and pH. There is no information of the actual DE of HG in twigs of the five species studied. A previous study, however, suggested that DE of HG may change largely in the course of the year as indicated by the fact that the ionic effect was largest in the winter in L. nobilis twigs. This was interpreted as possibly being due to the lowest amount of charged HG in this year period. High gelification can be induced in HG with high DE at pH
3 or, alternatively, at higher pH (5–7) on addition of Ca2+ (Tibbits et al., 1998). In this case, the pH of the tested fluids was 6.6 for deionized water and 7.4 for the commercial mineral water. No difference between the two fluids was recorded in terms of Kh for fully hydrated or embolized twigs of L. nobilis.
A final consideration is that classical literature reports that Ca2+ can be removed from pectates either at temperatures higher than 120 °C or through chelating agents like EDTA (Somers, 1973) or CDTA (Tibbits et al., 1998) at molar concentrations and ambient temperature. Hence, it is very unlikely that deionized water or solutions with high K+/Ca2+ ratio could elute Ca2+ from cell walls causing decrease in their porosity.
A different interpretation of the results of Van Ieperen and Van Gelder (2006) is proposed here. Their data clearly show that, in Chrysanthemum sp., the ion-mediated increase of Kh is maximized by only 1.5 mM KCl and about 1 mM CaCl2. Further increase of [KCl] in the perfused solution did not produce any variation in Kh. In the above cited paper, the ‘dose–response’ curve for ion-induced changes of Kh of P. laurocerasus is not reported. These data are, however, available in a recent paper by Gascò et al. (2007), where the ion-mediated increase of Kh with respect to deionized water was shown to be saturated at [KCl] of less than 5 mM. Hence, it is highly possible that 1 mM CaCl2 solution saturated the electrostatic screening of de-esterified groups of pit membrane pectins. In the present study, this view was confirmed in that Kh of fully hydrated Pr. laurocerasus twigs showed a strongly reduced response to 25 mM KCl when small amounts of Ca2+ were added to the reference solution (Fig. 2A). In the case of twigs of Pr. laurocerasus, C. siliqua, Ph. dioica, and Pe. gratissima, all with 50% loss of hydraulic conductance due to xylem embolism, 25 mM KCl induced a 55–100% increase of the residual Kh, regardless of Ca2+ was present or not in the reference solution (Fig. 2B). In embolized twigs, water is forced to cross a larger number of pits than in fully hydrated twigs, because embolized conduits have to be by-passed by the flowing solution. As a consequence, the ratio of axial-to-radial water flows is expected to be modified and 1 mM CaCl2 may no longer be sufficient to suppress the ion-mediated increase of Kh. In conclusion, it is felt that ion-mediated regulation of Kh cannot be ruled out and can still occur in planta as a possible mechanism to buffer cavitation-induced loss of water transport capacity (Gascò et al., 2006).
Experiments on L. nobilis twigs largely confirmed previous findings by Gascò et al. (2006, 2007) where the concentration-dependence of the Kh response to KCl was tested in the same species. It was shown that the ion-mediated increase of Kh was maximized at [KCl] between 50 mM and 100 mM. Because solute concentration of native xylem sap collected from fully hydrated twigs of L. nobilis turned out to be much lower than these values (about 20 mOsm kg–1, Tyree et al., 1999), one can expect that 0.5–1 mM Ca2+ in the reference solution (i.e. Ca2+ levels comparable to those recorded in native xylem sap; Table 2) did not alter the ion-mediated increase of Kh. In fact, this was the case in that 25 mM KCl caused Kh of fully hydrated laurel twigs to increase by about 20% regardless if Ca2+ was present or not in the reference solution. Experiments on L. nobilis also suggest that the reported suppression of ion-mediated flow changes (Van Ieperen and Van Gelder, 2006) was unlikely to be caused by elution of Ca2+ from cell walls. Instead, the discrepancy between our data and Van Ieperen and Van Gelder's data may simply reflect seasonal and/or species-specific differences in the DE of homogalacturonan (or other major compoinents of pectins) that is known to be under hormonal control and regulation and closely related to plant activity (Ren and Kermode, 2000).
In the present study, it was also confirmed that the residual Kh of embolized twigs of the species under study (PLC of about 50%) was strongly enhanced by 25 mM KCl (Fig. 1B). The eventual presence of Ca2+ together or not with a low concentration of other ions in the reference solution did not influence the Kh response. Tyree et al. (1999) have reported the xylem sap osmolality in L. nobilis twigs increasing from 20 mOsm kg–1 to about 50 mOsm kg–1 following cavitation, which would roughly correspond to a change from 10 mM to 25 mM KCl. Gascò et al. (2006) calculated that such an increase of ion concentration in the xylem sap of L. nobilis twigs would increase the residual Kh by about 50%. Ion secretion into xylem conduits has been shown to arise from radial phloem-to-xylem solute flow (Zwieniecki et al., 2004). Hence, it is very possible that substantial concentrations of inorganic ions may enrich sap and favour some compensation for cavitation-induced loss of Kh. This possibility provides a new interpretation of the experiments by Tyree et al. (1999), in that the reported increase in xylem sap osmolarity might reflect a compensation process operating in twigs following xylem cavitation.
Results of the present study suggest that the reported suppression of ion-mediated flow changes when Ca2+ is added to the reference solution (Van Ieperen and Van Gelder, 2006) cannot be regarded as a general phenomenon. Different species as well as different physiological status (fully hydrated versus embolized twigs) were shown to be factors causing different responses to ionic solutes in terms of the magnitude of the Kh increase as well as the eventual modulation of the phenomenon by Ca2+. Gascò et al. (2007) have reported that the extent of the ‘ionic effect’ can change dramatically on a seasonal basis. This might suggest that differences in the chemical nature of the prevailing pectins at the pit membrane level, as due to inter- and intra-specific variation, make the ion-mediated regulation of xylem hydraulics a largely variable and partially unpredictable phenomenon.
The actual occurrence and the extent of the ‘ionic effect’ in planta still awaits experimental confirmation. In our opinion, the most exciting perspective resides in the possibility that enrichment of xylem sap with inorganic ions following stem cavitation might transiently buffer the drop in xylem hydraulic conductance, thus allowing plants to maintain stomata open even when xylem water potential drops below critical values triggering xylem cavitation. New experiments describing in detail the eventual changes of xylem sap composition following cavitation on a diurnal and seasonal basis deserve more study and will probably be helpful to solve this issue.
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Acknowledgements |
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The visit of A Gascó to the Department of Biology, University of Trieste, was granted by Fundación Alfonso Martín Escudero.
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