Journal of Experimental Botany, Vol. 54, No. 383, pp. 825-833,
February 1, 2003
© 2003 Oxford University Press
Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use
Received 25 July 2002; Accepted 2 October 2002
1 Departamento de Citricultura y Otros Frutales, Instituto Valenciano de Investigaciones Agrarias, Moncada E-46113, Valencia, Spain
2 Departamento de Ciencias Experimentales. Universitat Jaume I. Campus Riu Sec. E-12071 Castellón, Spain
3 To whom correspondence should be addressed. Fax: +34 6 1390240. E-mail: mtalon{at}ivia.es
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Abstract |
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In this work, seedlings of two citrus rootstocks, the salt-tolerant Cleopatra mandarin (Citrus reshni Hort. ex Tan.) and the salt-sensitive Carrizo citrange (Citrus sinensis [L.] Osb. x Poncirus trifoliata [L.] Raf.) were used to study the relationship between chloride and water uptake. The results indicated that net chloride uptake rates in both genotypes were alike and decreased linearly with the time of salinity exposure, although they were more rapidly reduced in the tolerant genotype. In each rootstock, chloride uptake rates paralleled the decreases in transpiration rates. When transpiration was modified, concomitant changes in leaf Cl– concentrations were observed. There was a high positive correlation between total chloride content per plant and total water absorbed. In addition, the data indicate that the tolerant genotype ‘excluded’ more chloride, i.e. it absorbed lower amounts of chloride per volume of water. Cleopatra also possessed a less efficient root system for water uptake and a higher shoot-to-root ratio. The results show that, overall, chloride absorption is linked to water use and that further tolerance in Cleopatra is mostly conferred by superior root resistance to Cl– uptake. Therefore, it is proposed that chloride absorption and, hence, salt tolerance in citrus depends to a great extent upon water use.
Key words: Chloride uptake and distribution, salinity, sodium chloride, transpiration, water absorption.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In citrus, the physiological disturbances produced by salinity are associated with leaf chloride build-up rather than with sodium accumulation (Romero-Aranda et al., 1998). Thus, the capability of citrus plants to tolerate salinity is thought to be intimately related to the ability of the rootstock to exclude chloride (Cooper et al., 1952; Walker et al., 1983; Bañuls et al., 1997), although the nature of this mechanism remains totally unresolved (Storey and Walker, 1999).
Analyses of elution curves of isotope suggested that citrus roots might posses a major passive uptake component and a very feeble active system of Cl– uptake (Altman and Mendel, 1973). Passive Cl– influx into cells and into the root xylem might occur at high external Cl– concentrations (Cram, 1973; Binzel et al., 1988). Under these conditions, it is possible for the membrane potential to be less negative than the Cl– equilibrium potential allowing for a passive influx (Skerrett and Tyerman, 1994). Chloride ions may enter cells through channels, such as the chloride outward rectifiers (ClOR) (Tyerman et al., 1997; Tyerman and Skerrett, 1999) and other non-selective anion channels. Moreover, several members of the chloride channel family (ClC), originally identified in animals, have been cloned in plants (Lurin et al., 1996; Hechenberger et al., 1996). Carriers of other anions might also facilitate Cl– uptake (Logan et al., 1997).
On the other hand, circumstantial observations in citrus suggest that chloride root uptake and subsequent accumulation in leaves could be dependent upon water absorption and transpiration. With the exception of Rangpur lime (Storey, 1995), it appears that changes in relative humidity may modify leaf Cl– levels in other citrus species (Storey, 1995; Elgazzar et al., 1965; Walker, 1986; Walker et al., 1990). Furthermore, it has been reported that the growth habit and the plant morphology are crucial factors in salt tolerance (Altman and Mendel, 1973; Moya et al., 1999). Relationships between vigour, water use and salt absorption are also apparent in published experiments from previous work. Thus, the rootstock ranking of chloride tolerance appears to reflect, in general, its water use (Syvertsen et al., 1989). Finally, in a previous report it has been shown that chloride uptake under salinization is mostly driven by passive forces, suggesting that chloride root uptake might certainly be linked to water absorption (Moya et al., 1999). In spite of this information, no conclusive or compelling evidence linking chloride uptake to water absorption has been presented so far. In this work, chloride salt-sensitive (Carrizo citrange) and salt-tolerant (Cleopatra mandarin) citrus rootstocks have been used to show that chloride uptake, and hence salt tolerance, is dependent upon water use.
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Materials and methods |
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Plant material
The experiments described in this work were performed with 2-year-old seedlings of the citrus rootstocks Carrizo citrange (Citrus sinensis [L.] Osb. x Poncirus trifoliata [L.] Raf.) and Cleopatra mandarin (Citrus reshni Hort. ex Tan.). In general, Carrizo seedlings exhibit vigorous growth, taller phenotypes and medium-to-high sensitivity to salinity, while Cleopatra seedlings are slower growing plants showing moderate apical dominance and high tolerance to salt conditions (Wutscher, 1979). Plants were grown under glasshouse conditions until the beginning of the experiments. To confirm that the trends in the responses were similar in seedlings and adult plants, 12-year-old field trees of Carrizo and Cleopatra, situated in the experimental orchard of the IVIA, were utilized in complementary experiments.
Growth conditions
Environment chamber conditions: At the beginning of the experiments, plants were removed from the commercial soil medium and carefully washed in order to eliminate solid particles. Plants were then transferred to black-painted plastic pots containing 2.0 l of nutrient medium vigorously aerated with a Simcos air pump model K-350. Plants were placed in controlled environment chambers (Conviron model E15 CPM3244) with a photoperiod of 16 h light at 26 °C and 70% relative humidity, and 8 h darkness at 19 °C and 80% relative humidity. The photosynthetic photon flux density (PPFD) at the leaf zone was 250 µmol m–2 s–1. The composition of the hydroponic medium was previously described in detail (Moya et al., 1999). During the experimental periods, plants of both rootstocks developed new and healthy roots.
After an acclimatization period of at least 7 d in the nutrient medium, plants were transferred to 25 cm long x 5 cm wide glass tubes, protected with aluminium foil to avoid alga proliferation. The glass tubes contained 100 ml of the nutrient solution supplemented with increasing concentrations of NaCl (30, 60, 120, 180, and 240 mM). Each glass tube had one single plant with the aeration system described above. Salt treatments were given for one month.
Glasshouse conditions: To study the influence of water absorption on chloride uptake, transpiration rates were either increased through partial defoliation (Moya et al., 1999) or decreased via split root manipulation (Davies and Zhang, 1991). Defoliation was more severe in Cleopatra (80%) than in Carrizo (60%). There was no growth of new leaves during the length of the experiments. Roots were partially dried placing approximately 80% of the root system under dried air into impermeable plastic bags. Maximum and minimum temperatures during the night were 19–17 °C and during the day 29–24 °C. Relative humidity during night and day fluctuated between 40% and 85%.
After an acclimatization period of at least 7 d in the nutrient medium as above, plants were transferred to 1.0 l plastic bottles filled with the nutrient solution supplemented with 60 mM NaCl. Bottles were sealed with plastic around the stem to avoid evaporation. The amount of water absorbed was determined by weight differences. Transpiration per unit of time and leaf area was then calculated. The saline treatment was maintained for 14 d.
Net chloride uptake rates
Net chloride uptake rates were determined measuring chloride depletion in the media as previously described (Moya et al., 1999). During the whole experimental period, the volume of the tubes was made up to 100 ml daily with distilled water, and two aliquots of 0.130 ml each were taken. No visible symptoms of salt damage were observed in these plants. Their chloride contents were determined by the silver ion-titration method with a Corning 926 automatic chloridometer (Corning Ltd. Halstead Essex, UK) according to Gilliam (1971), as explained in Romero-Aranda et al. (1998). For each single plant, a graph showing the relation between the decrease in chloride concentration in the nutrient medium with time was plotted. Chloride absorption rates were calculated from the slopes of these relationships.
Chloride content in plants
After saline treatments, plants were harvested and washed. Roots, stems and leaves were separated and freshly weighed. The different organs were oven-dried for at least 72 h at 70 °C and the dry weight was determined. The dry material was ground to a powder and chloride concentration was determined by silver ion-titration as above. The Cl– quantities present in plants before salt treatments were determined and then subtracted to calculate the Cl– amounts specifically absorbed during treatments.
Root water transport (sap flow)
Root capacity for water transport was determined using a Soilmoisture pressure chamber (Model 3000; Soilmoisture Equipment Corp., Santa Barbara, CA, USA). Plants were cut 5 cm above the first root, and roots were placed into the pressure chamber cylinder with the cut end outside of the cylinder. The root system was submerged in nutrient solution, and a plastic tube was connected to the cut end of the stem to collect the fluid. A pressure of 0.36 MPa was applied, and the fluid was recovered every 10 min in different recipients. The fluid was weighted to determine the volume extruded.
Gas exchange measurements
Net photosynthesis and transpiration rates in outdoors growing plants and tress were measured with a LI-6200 portable photosynthesis system (Li-Cor Inc., Lincoln, NE, USA) using a 250 ml cuvette. Determinations were performed during the morning (07.30–09.30 h) to avoid elevated afternoon temperatures and higher vapour pressure deficits. During measurements, radiation within the cuvette was supplemented with a 150 W lamp (Philips EFR A1/232) after cooling with circulating cold water and external fans. All measurements were performed at photosynthetic photon flux density (PPFD, 400–700 nm) of 900–1000 µmol m–2 s–1, which exceeds saturating photosynthetic photon flux for citrus. Five to ten fully expanded matured leaves per treatment were used for measurements.
Stomatal density
The abaxial surface of the leaf was painted with nail varnish to obtain a transparent surface mould. This dry film was carefully separated and placed in a micro slide covered with a cover glass. Measurement of stomata number per unit of leaf surface was conducted in a Leitz-Orthoplan microscope (Leitz, Wetzlar, Germany).
Light microscopy
Twelve 2x3 mm pieces from roots of different plants were fixed, dehydrated and embedded in LR White (London Resin Co., Woking, Surrey, UK) according to Tadeo et al. (1997). Semi-thin transverse sections (1 µm thickness) were cut with a Leica RM2165 Rotary Microtome (Leica Instruments, Heidelberg, Germany) and stained with toluidine blue O (CI 52040, Merck, Darmstad, Germany) after O’Brien et al. (1964). Representative sections were also examined and photographed with a Leitz-Orthoplan microscope.
Statistical analyses
Parameters were compared using analyses of variance and Newman-Keuls multiple range tests (P <0.05). Relationships between parameters were investigated using linear and exponential regression analyses where appropriate.
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Results |
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Leaf chloride concentration and transpiration rates are higher in the salt-sensitive genotype
It is known that the salt-sensitive rootstock, Carrizo citrange, accumulates in leaves higher Cl– amounts than the salt-tolerant Cleopatra mandarin (Romero-Aranda et al., 1998), a difference that could be detected even in non-salinized seedlings or adult trees (Table 1). In these plants, net photosynthesis and transpiration was about 20–30% higher in Carrizo than in Cleopatra. Higher transpiration rates were measured in trees probably due to high vapour pressure deficits found outdoors (in general, 0.15 versus 0.90 Pa). The data also showed that these changes were not due to differences in stomatal density. In the following experiments, the relationship between Cl– absorption and transpiration was studied.
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3) within each column followed by the same letter do not differ significantly at P <0.05.
Salt exposure reduced net chloride uptake rates
Under saline treatments (30–240 mM NaCl) the two rootstocks showed a similar behaviour regarding root chloride uptake. In both genotypes, net chloride uptake rates decreased with time (Fig. 1). These changes were calculated from the decrease in chloride concentration in the nutrient medium (Moya et al., 1999). At the beginning of treatments, uptake rates were slightly higher for Cleopatra (for example, 87.6 versus 122.2 µg g–1 root dry weight h–1 at 180 mM) and then, they gradually decreased in both during salt exposure. This reduction was not only due to Cl– depletion in the nutrient medium, since, in both rootstocks, net chloride uptake rates after several days of treatment at high NaCl concentrations were clearly lower than those observed at the onset of the treatments at low NaCl. For example, in Carrizo, chloride concentration in the external medium after 20 d of treatment with 60 mM NaCl was 43±3 mM and net chloride uptake rate was 9.82 µg g–1 root dry weight h–1. However, in plants treated with 30 mM NaCl chloride uptake rate at day 0 was 17.6 µg g–1 root dry weight h–1. Similar pattern of changes was found in Cleopatra. This observation clearly showed that salt exposure reduced net chloride uptake rates
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The reduction of chloride uptake rates was faster in Cleopatra than in Carrizo, since the slope values, in abso lute terms, for regression lines were higher in Cleopatra (for example, –6.14 versus –4.77 at 240 mM NaCl).
The decreases in both chloride uptake and transpiration rates are coincident
The relationship between chloride uptake and transpiration rates was studied in plants of Carrizo and Cleopatra grown under 60 mM NaCl. Two sets of plants of similar and uniform size growing under the same environmental conditions were used for that purpose. In one set, Cl– uptake rates were determined during one month, while in the second set transpiration was measured for 14 d. The data of this experiment indicated that, in the two genotypes, both rates decreased in a related manner. However, the chloride uptake rate reduction was clearly linear, whereas the transpiration rate decline appeared to show a minor ‘negative exponential’ effect. To elucidate the linearity versus the exponential pattern of change of the transpiration rates, these measurements were repeated 4-fold in independent plants to generate new curves. The data showed that in seven out of the 10 curves generated, the r2 of the exponential pattern was slightly higher than that of the linear one. Although all sets of data are not presented here, Fig. 2 shows typical results obtained with intact plants. In this figure, chloride uptake and transpiration rates in Carrizo decreased following the equations Y= –1.047X+30.868 (r2=0.999) and Y=6.0005e–0.0453x (r2=0.976), respectively. According to the equations, chloride uptake was arrested at 29.5 d (when Y=0, X=29.5, in the first equation) and transpiration tended to decline to a minimum and constant value. In Cleopatra, the equations were Y= –1.266X+30.450 (r2=0.999) and Y=2.4178e–0.0576x (r2=0.977), respectively, and chloride uptake was arrested at 24.1 d (when Y=0, X=24.1) and transpiration, as above, tended to a minimum value. This indicates that the decreases in both chloride uptake and transpiration rates are rather coincidental.
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Leaf chloride concentration parallels leaf transpiration rate
To study the relationship between transpiration rate and Cl– content, two different sets of experiments involving manipulation of transpiration were performed on plants of both genotypes grown at 60 mM NaCl. In the first set, transpiration rates could not be modified efficiently by changing the environmental relative humidity. In the second group of experiments, however, transpiration was severely altered through partial defoliation and root confinement. Both sets of experiments essentially showed the same results, although a higher statistical significance between chloride content determinations was reached in the second group of experiments, the one that produced wider transpiration differences (Table 2).
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In all treatments, transpiration decreased as explained above (data were registered during the 14 d period of study, although only the initial determinations at day 4 are presented in Table 2). In all treatments (control, defoliation, and root confinement), higher transpiration rates were always observed in Carrizo. For the two genotypes, plants with reduced root systems had the lowest transpiration, while intact plants showed intermediate values. Partial defoliation increased the transpiration rates of the remaining leaves, a process previously reported in citrus (Moya et al., 1999), and it was proportional to the magnitude of leaf removal. Thus, leaf area in Carrizo was reduced by 60% and transpiration in the remaining leaves increased approximately 2.5-fold. In Cleopatra, 80% of the leaves were removed and transpiration increased 5-fold. In general, Carrizo also had higher concentrations of leaf chloride (Table 2). In both genotypes, defoliated plants showed the highest leaf chloride contents, whereas plants with a confined root system showed the lowest. Therefore, changes in leaf chloride concentrations paralleled those of leaf transpiration rates.
In both rootstocks, total chloride per plant, however, was similar in defoliated and intact plants, and lower in plants with reduced root systems. This observation indicated that total chloride absorbed per plant was not necessarily linked to leaf transpiration rates.
Total chloride content correlates with total water absorbed
In all plants analysed in the previous experiments, the data showed an apparent relationship between total chloride content per plant and total water absorbed during the salinization period. The dependence of chloride build-up upon water absorption could be exemplified with positive linear regressions of high statistical significance (Fig. 3). Both rootstocks showed linear relationships (P <0.001 in Carrizo and P <0.01 in Cleopatra) between total water uptake and total chloride absorbed during the saline treatment. Similar relationships between total water and absolute chloride contents in roots, stems or leaves were also observed (data not shown). In all regressions, the slope was higher in Carrizo (about 1.5-fold) than in Cleopatra, indicating that the salt-sensitive genotype absorbed higher amounts of Cl– per volume of water.
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0.001 (Carrizo) and P The salt-sensitive genotype possesses a more efficient root system for water uptake and a lower shoot-to-root ratio
In seedlings of similar size and weight, the ability of the root to transport water was higher in the salt-sensitive genotype (Table 3). When roots were exposed to 0.36 MPa pressure, for example, the amount of xylem fluid collected per unit of time in the stem sections was 1.7-fold higher in Carrizo than in Cleopatra (38.7 versus 23.0 µl min–1). Accordingly, light micrographs of roots revealed that both size and number of xylem elements were superior in Carrizo (Fig. 4). Therefore, the sensitive rootstock had a more efficient root system for water uptake and transport.
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In both rootstocks, the percentage of younger roots having high uptake capabilities (diameter <2 mm) was very similar (Table 4). The chloride content in roots from non-salinized seedlings of both genotypes was also alike and these amounts were superior in the younger roots (7 versus 4 mg g–1 DW). The ratio between total leaf area and dry weight of the younger roots was 3-fold higher in Cleopatra (235 versus 80 cm2 g–1 root DW). This indicates that, in plants with the same leaf area, the root system is 3-fold larger in the sensitive rootstock.
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Discussion |
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In many studies on salt tolerance it has not been possible to determine whether the toxic effects observed are due to Cl–, Na+ or to a contribution of the two. During the last decades many efforts on this subject have been centred on the sodium effects, while the role of Cl– has been scarcely investigated (Greenway and Munns, 1980). Thus, it is not surprising that the literature on Cl– uptake, effect or involvement in toxicity is extremely small (Pasternak, 1987; Munns, 1993). Actually there are only a few species (grapes, barley, soybean, and citrus) that have been conclusively reported to be more sensitive to chloride than to sodium.
In citrus, many physiological and anatomical disturbances produced by salinity are linked to leaf chloride build-up rather than to sodium accumulation (Bañuls et al., 1997; Romero-Aranda et al., 1998). It has recently been shown that Cl– uptake under salinity is driven by passive forces depending upon the morphological relationships between shoots and roots (Moya et al., 1999). In the present work, evidence is reported that in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin rootstocks, chloride uptake and accumulation and, therefore, salt tolerance, are related to water use. The process is essentially characterized with three findings: first, net chloride uptake rates increased with external NaCl, although decreased with time independently of the salt concentration (Fig. 1). Secondly, Cl– uptake and transpiration rates decreased in a parallel manner during the salinization period (Fig. 2). Finally, through defoliation and split root manipulation, it is shown that changes in leaf Cl– concentration were concomitant with changes in leaf transpiration rate (Table 2), while total water and total Cl– absorbed per plant (Fig. 3) were highly correlated. It is worth mentioning that citrus are plants that readjust efficiently to osmotic stresses and to environmental humidity changes and that, in general, it is not possible to obtain, by modifying air humidity, transpiration differences higher than 35–40%. However, the combination of defoliation and dried roots provided clear-cut differences (up to 6-fold increases) in transpiration rates, a necessary experimental scenario to ascertain the relationship between Cl– uptake and transpiration rates. The mechanism that regulates transpiration in these manipulations also appears to be dependent on ABA, since it is known that defoliation decreases ABA (Neales and McLeod, 1991; Huang et al., 1991) and that drying part of the roots in non-watered soil increases ABA (Neales et al., 1989). Furthermore, drying part of the roots in dry air has a faster and more intense effect on ABA (Davies and Zhang, 1991).
Taken together, those three findings suggest that Cl– uptake and accumulation, the parameters responsible for salt damage in citrus might be linked to water use. Based on the data presented above, the higher chloride amounts found in the sensitive genotype, compared with the tolerant one (Tables 1, 2; Grieve and Walker, 1983; Zekri and Parsons, 1992; Zekri, 1993; Romero-Aranda et al., 1998) are partially due to differences in water use, rather than to differences in chloride uptake rates. Thus, Carrizo shows higher ability for water uptake and transport (Table 3; Fig. 4) and greater rates of leaf transpiration in both normal (Table 1) and saline (Table 2; Fig. 2) conditions. If it is assumed that the amounts of chloride and water absorbed are linked, rootstocks that use more water may also permit higher chloride influxes. Thus, it has been reported that salt-tolerant rootstocks use less water than the sensitive ones (Syvertsen et al., 1989).
Furthermore, transpiration under saline stress decreased faster in Cleopatra (Fig. 2), indicating that some tolerance responses to salt stress (i.e. readjustments to progressive reductions of Cl– uptake) took place more rapidly in the tolerant rootstock. Transpiration reductions observed under saline conditions (Behboudian et al., 1986; Graham and Syvertsen, 1989; Walker et al., 1990; Storey, 1995) may be due to ABA regulation (Gómez-Cadenas et al., 1998) of stomatal closure (Walker et al., 1993; Bañuls and Primo-Millo, 1992, 1995; Bañuls et al., 1997), the appearance of root injuries and/or decreases in root hydraulic conductance (Swietlik, 1989; Zekri and Parsons, 1989).
The hypothesis that chloride accumulation in leaves is linked to transpiration rates may have additional consequences for tolerance, i.e. the dilution of chloride by growth could be significant. Thus, the same amount of Cl– absorbed may result in higher leaf concentrations in Carrizo than in Cleopatra since, in the latter, the shoot-to-root ratio is 3-fold higher (Table 4; Moya et al., 1999). An illustrative example of this effect is provided by data from partial defoliated plants in Table 2. When leaves were removed, transpiration rates increased proportionally to the magnitude of the leaf removal and, therefore, total transpiration or total water absorbed did not change. The data showed, confirming a prediction of the proposal, that total chloride absorbed in defoliated and intact plants was similar. This implies that net chloride uptake rates were not essentially modified in defoliated plants, although leaf transpiration rates and, therefore, leaf chloride concentrations increased.
Finally, an additional adaptive improvement of Cleopatra to salt tolerance can be inferred from Fig. 3 that shows that although total chloride and water are linearly related in both genotypes, the slope of this relationship is lower in Cleopatra. This observation suggests that the tolerant roots ‘exclude’ more chloride, i.e. they absorb lower amounts of chloride per volume of water. Thus, it appears that Cleopatra, compared with Carrizo, possess a more restrictive mechanism for chloride influx at the root level. The nature of this adaptative mechanism and its physiological significance regarding salt tolerance in citrus are not known, but certainly deserve further investigation.
The hypothesis that Cl– uptake might depend upon water absorption is not totally new, although strong evidence for a cause–effect relationship has not been presented before. In their review of the relevant literature, Storey and Walker (1999) reached the conclusion that chloride accumulation in citrus could certainly be a transpiration-dependent phenomenon. In the present work, evidence is presented that in the sensitive Carrizo and the tolerant Cleopatra, chloride and water uptake are directly linked, and that transpiration rates very likely determine the leaf chloride amounts.
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Acknowledgements |
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JL Moya was the recipient of a Ministerio de Educación y Ciencia predoctoral fellowship. This work was supported by the CICYT and INIA through grants No. AGF94-0946-C03-01 and SC97-106, respectively, to MT.
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