JXB Advance Access originally published online on March 3, 2003
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Journal of Experimental Botany, Vol. 54, No. 385, pp. 1281-1288,
April 1, 2003
© 2003 Oxford University Press
Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation?
Received 10 December 2002; Accepted 19 December 2002
1 Department of Botany, The University of Queensland, Brisbane, QLD 4072, Australia
2 Natural Sciences Academic Group, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616
3 Present address and to whom correspondence should be sent: Department of Biological Sciences, IENS, University of Lancaster, Lancaster LA1 4YQ, UK. Fax: +44 (0)1524 843854. E-mail: I.Dodd{at}lancaster.ac.uk
Abbreviations: AX, artificial xylem (solution); gs, stomatal conductance; 
shoot, shoot water potential.
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Abstract |
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Stomatal conductance (gs) of pepper (Capsicum annuum L.) plants decreased during the second photoperiod (day 2) after withholding nitrate (N). Stomatal closure of N-deprived plants was not associated with a decreased shoot water potential (
shoot); conversely shoot was lower in N-supplied plants. N deprivation transiently (days 2 and 3) alkalized (0.2–0.3 pH units) xylem sap exuded from de-topped root systems under root pressure, and xylem sap expressed from excised shoots by pressurization. The ABA concentration of expressed sap increased 3–4-fold when measured on days 2 and 4. On day 2, leaves detached from N-deprived and N-supplied plants showed decreased transpiration rates when fed an alkaline (pH 7) artificial xylem (AX) solution, independent of the ABA concentration (10–100 nM) supplied. Thus changes in xylem sap composition following N deprivation can potentially close stomata. However, the lower transpiration rate of detached N-deprived leaves relative to N-supplied leaves shows that factors residing within N-deprived leaves also mediate stomatal closure, and that these factors assume greater importance as the duration of N deprivation increases. Key words: Abscisic acid, Capsicum, nitrate, stomata, water status, xylem pH.
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Introduction |
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The sudden withdrawal of nitrate (N) from the plant rhizosphere can decrease stomatal conductance (gs) within 48 h (Chapin et al., 1988). Both hydraulic and non-hydraulic mechanisms have been considered to elicit stomatal closure. N deprivation decreases root hydraulic conductivity (Radin and Boyer, 1982; Chapin et al., 1988) and may decrease leaf water potential (Radin and Parker, 1979) and turgor (Radin and Boyer, 1982), which may directly close stomata. However, stomatal closure following N deprivation can occur without changes in leaf water potential (Chapin et al., 1988), suggesting that stomatal closure may result from changes in the delivery of chemical signals from the root system, in an analogous manner to the effects of water stress (Chapin, 1990; Clarkson and Touraine, 1994).
One of these signals could be the plant hormone abscisic acid (ABA). Although N deprivation increased the ABA concentration of xylem sap allowed to exude under root pressure (Goldbach et al., 1975; Krauss, 1978), xylem sap collected by pressurization of de-topped root systems showed no effect of N deprivation on ABA concentration (Palmer et al., 1996; Zdunek and Lips, 2001). However, increased xylem sap ABA concentration may not always be necessary for ABA-induced stomatal closure to occur. N deprivation increased the sensitivity of detached cotton leaves to ABA supplied via the xylem (Radin et al., 1982) such that N-deprived leaves showed stomatal closure at xylem sap ABA concentrations typically found in vivo.
Recent work has shown that alkalization of xylem sap is a common response to various environmental stresses (Wilkinson and Davies, 2002) and that supplying detached leaves with alkaline buffers via the transpiration stream can close stomata (Wilkinson and Davies, 1997; Wilkinson et al., 1998). The ability of an alkaline artificial xylem (AX) solution to close stomata was ABA-dependent, as leaves detached from an ABA-deficient mutant did not show decreased transpiration in response to alkaline pH unless a low concentration of ABA (typical of that found in well-watered plants) was also supplied in the AX solution (Wilkinson et al., 1998). Changes in nitrate nutrition can also alter xylem sap (Kirkby and Armstrong, 1980) and leaf apoplast pH (Dannel et al., 1995), and may therefore close stomata.
The objectives of this study were to determine whether stomatal closure of N-deprived plants could be attributed to altered leaf water relations and/or xylem-borne signals (pH and/or ABA concentration). Detached leaf transpiration bioassays were used to assess the physiological significance of the observed changes in xylem sap composition. Pepper (Capsicum annuum L.) was chosen as preliminary studies showed that stomatal conductance of this species responded sensitively to N deprivation.
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Materials and methods |
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Plant culture
Pepper (Capsicum annuum L. cv. Californian Wonder) seeds were germinated on moistened filter paper (Whatman No. 1) in the dark at 25 °C for 1 week, then transplanted into 1270 cm3 plastic cylindrical pots (90 mm diameter, 200 mm long) filled with a sand:perlite (4:1, v:v) mixture. A perforated plastic plate was taped over the base of the pots to retain the growth medium and assist drainage. Pots were maintained under natural daylight in a temperature controlled greenhouse (28/23 °C day/night) at the University of Queensland. Pots were given 80 cm3 of a complete nutrient solution [composition (in mM) KNO3, 2; Ca(NO3)2.4H2O, 1.5; KH2PO4, 1; MgSO4.7H2O, 2; (in µM) NaFeEDTA, 71.4; H3BO3, 5; MnCl2.4H2O, 0.5; ZnSO4.7H2O, 0.2; (NH4)6Mo7O24.4H2O, 0.1; CuSO4.5H2O, 0.2] every week for 3 weeks, then twice a week for 1 week. When the experiments commenced, plants had visible floral buds but not sympodial branches, 8–9 leaves apparent and a mean (±SE) leaf area of 94±5 cm2.
Three days prior to the start of each experiment, plants were moved into a controlled environment chamber at a photosynthetic photon flux density of 200–300 µmol m–2 s–1 at plant height and a 9 h photoperiod. Day/night cabinet temperatures were 28/23 °C, giving average ambient day and night VPDs of 2.2 kPa and 0.6 kPa, respectively.
Before the start of the photoperiod on the first day of each experiment, all pots received 320 cm3 of tap water to leach away any residual nutrient solution. Then half the pots received 240 cm3 of the complete nutrient solution described above (N-supplied), while the remainder (N-deprived) received 240 cm3 of an iso-osmotic nitrate free solution in which nitrate was replaced by chloride and the cations were unchanged. Even though N deprivation using chloride and sulphate as counter-ions yields similar physiological effects (Mattsson et al., 1988), chloride was chosen in preference to sulphate as a counter-ion since it is not metabolized and it will be compartmentalized into the vacuole. Furthermore, applying 10 mM chloride as NaCl (double the chloride concentration applied to N-deprived plants here) to 22-d-old Capsicum plants for 6 weeks had no effect on leaf area or dry weight (Chartzoulakis and Klapaki, 2000). N treatments were randomly allocated to plants within the controlled environment chamber. Following irrigation, the pots were covered with a layer of white plastic beads to minimize surface evaporation. Transpirational losses were replaced daily at the start of the photoperiod.
Physiological measurements
Whole plant transpiration rates were determined gravimetrically by weighing pots at the start and end of the photoperiod. The lengths of growing leaves were measured at the start of the photoperiod with a piece of graph paper photocopied onto acetate. At the end of the experiment, the length and area of all leaves was determined using image analysis (DIAS 1.12, Delta-T Devices, Burwell, UK). Daily transpiration rates were calculated on the basis of leaf area by using regressions of leaf area on length.
Abaxial stomatal conductance (gs) was measured using a porometer (AP4, Delta-T Devices, Burwell, UK) at various times during the photoperiod.
During the middle 3 h of the photoperiod, the water potential (shoot) of the entire shoot (excised 5 mm above the cotyledons) was determined using a Scholander-type pressure bomb (Plant Moisture Systems, Santa Barbara, CA, USA) where the chamber was lined with moistened filter paper. The pressure bomb was located adjacent to the controlled environment chamber so that the time between shoot excision and sealing the shoot into the pressure bomb was less than 10 s. Following measurement of shoot, the cut surfaces of both the shoot and the remaining stump were rinsed with distilled water and blotted dry. Xylem sap was collected from the shoot at 0.5 MPa above the balancing pressure for 3–5 min. Sap issuing from the cut stump of the plant under root pressure was collected for 1 h. Saps were collected via glass capillaries into eppendorf tubes, then frozen in liquid nitrogen and stored at –80 °C until analysis.
Nitrogen analysis
On day 0 (prior to imposition of N treatments) and day 4 (the end of the experiment), leaves at node 7 were excised during the middle 3 h of the photoperiod, then oven-dried at 80 °C for 2 d. Leaves were ground to a fine powder, then 0.01 g aliquots taken for determination of total N and nitrate concentration.
Dried leaf tissue was placed in a digestion tube with a Kjeldahl tablet and 5 cm3 of concentrated sulphuric acid (H2SO4). The mixture was heated at 250 °C until it turned clear and the clear solution was used for N determination using an autoanalyser (Model 1030, Kjeltec, Höganäs, Sweden).
Dried leaf tissue was ground using a pestle and mortar with 5 cm3 of deionized water and then incubated at 37 °C for 2 h. Nitrate concentration was determined using a flow injection analyser (QuikChem 800, Lachat Instruments Inc, Milwaukee, USA) which employed the nitrite colorimetric reaction with cadmium as the reducing agent. Nitrite was formed by passing the sample through a copperized cadmium column, then diazotized with sulphanilamide and coupled with N-(1-naphthyl)ethylenediamine dihydrochloride after which the absorbance of the mixture was determined at 540 nm.
Measurement of xylem sap constituents
Xylem pH was measured with a microelectrode (Model 98–02 BN, Orion Instruments, Boston, MA, USA) interfaced with a pH meter (Model 900I3, TPS Ionode, Brisbane, Australia).
Twenty nanograms of [2H6] ABA were added to each sap sample. Samples were evaporated to dryness under vacuum, redissolved in 20 mm3 of methanol, then diazomethane added to methylate ABA. Samples were then dried, redissolved in 250 mm3 of water and partitioned three times against 200 mm3 diethyl ether. The diethyl ether was removed under N2, and the sample dissolved in chloroform for injection into the GC-MS. Quantification of ABA was performed as in Batge et al. (1999) using the ion ratio 194:190.
Detached leaf transpiration assays
Leaves were detached from both N-deprived and N-supplied plants using several batches of plants grown as above. Leaves (with petioles attached) at the top and base of the plant were detached at the junction of the node prior to the start of the photoperiod, recut under distilled water and then placed in eppendorf tubes containing 1.5 cm3 of an artificial xylem (AX) solution. The composition of the AX solution was (in mM): CaCl2, 1; KH2PO4, 1; K2HPO4, 1; MnSO4, 0.1; and MgSO4, 0.1 for all leaves. Leaves detached from N-supplied plants were also supplied with 3 mM KNO3 while leaves detached from N-deprived plants were also supplied with 3 mM KCl. Solutions were buffered to specified pHs by the dropwise addition of either 1 M HCl or KOH, and contained either 10 or 100 nM abscisic acid. In a separate experiment, the effect of a synthetic cytokinin, 0.5 µM benzyladenine, was assessed. The vials were randomized within the growth cabinet and weighed on an analytical balance at 1–2 h intervals. After 6 h, leaf area was determined as described previously, to calculate transpiration rates on the basis of leaf area.
Statistics
Significant differences in shoot water potential, stomatal conductance, transpiration rate and xylem sap composition between N treatments were discriminated using Student’s unpaired t-test. Effects of different artificial xylem solutions on detached leaf transpiration rate were detected using ANOVA, with means separated by Tukey’s HSD (P <0.05).
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Results |
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Prior to the imposition of N treatments (day 0), leaves at node 7 had a mean total nitrogen concentration of 71 mg g–1 DW, including a nitrate concentration of 5.7 mg g–1 DW (Table 1). After 4 d, leaf total nitrogen concentrations had declined by 17% and 41% in N-supplied and N-deprived plants, respectively. Leaf nitrate concentrations increased in N-supplied plants, but had dropped to barely detectable concentrations in N-deprived plants.
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Photoperiod transpiration rate of the whole plant did not significantly decline in response to N deprivation until the third photoperiod after treatment (Fig. 1a). However, measurements of individual leaves showed that stomatal conductance decreased towards the end of the second photoperiod (Fig. 2b), and became more pronounced the following day (Fig. 2c).
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Shoot water potentials did not significantly differ until day 3 (Fig. 1b), when
shoot of N-supplied plants was 0.1 MPa less than N-deprived plants. The decreased shoot of N-supplied plants was a consequence of their greater transpiration rate (Fig. 1a), as enclosing shoots in plastic bags for 30 min (to reduce transpiration) prior to water potential determination eliminated differences between N treatments (data not shown). Root exudate of N-deprived plants was significantly more alkaline by no more than 0.3 units on days 2 and 3 (Fig. 1c). Sap expressed from the shoot under pressure followed a similar pattern, although treatments statistically differed only on day 3. Shoot xylem sap was more alkaline than root exudate. When similar experiments were performed in the greenhouse, root exudate of N-deprived Capsicum and sunflower plants was also more alkaline (data not shown). N deprivation significantly increased xylem sap ABA concentration when measured on days 2 and 4 (Table 2).
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Transpiration rates of detached leaves remained reasonably stable throughout the photoperiod in all treatments (data not shown), thus time-courses are not presented. Instead, data are summarized according to treatment (Fig. 3). On day 2, transpiration rates of detached leaves showed similar responses to alterations in artificial xylem (AX) solution composition, irrespective of leaf age and N treatment (Fig. 3). Increasing the ABA concentration fed from 10 nM to 100 nM generally had no significant effect on detached leaf transpiration, except in older N-supplied leaves fed AX solution at pH 6 (Fig. 3d). Increasing the pH of the AX solution decreased transpiration rates of all leaf types, although the magnitude of the pH response was diminished in older leaves (cf. Fig. 3a, c and Fig. 3b, d). Detached leaves responded similarly to changes in xylem-supplied ABA and pH on both days 2 and 4 (data not shown).
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Older leaves detached from N-deprived plants showed a 31% decrease in transpiration rate compared to leaves detached from N-supplied plants (cf. Fig. 3c, d) even when fed an ‘optimal’ artificial xylem solution (pH 6, 10 nM ABA). This difference was magnified on day 4 such that the mean (±SE) transpiration rate of old N-deprived leaves (0.23±0.02 mmol m–2 s–1, n=8) was 75% less than old N-supplied leaves (0.91±0.05 mmol m–2 s–1, n=8). Supplying a synthetic cytokinin (0.5 µM benzyladenine) in the AX solution did not increase detached leaf transpiration rate (Table 3).
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Discussion |
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N deprivation induced stomatal closure (Fig. 2) of Capsicum leaves without any decrease in shoot water status. In contrast to the decreased midday leaf water potential of N-deprived cotton leaves (Radin and Parker, 1979), N deprivation either increased (when measured in transpiring plants; Fig. 1b) or had no effect on (when measured under conditions of low transpiration) Capsicum shoot water potential. Non-hydraulic explanations for stomatal closure were considered.
Many reports indicate a negative relationship between xylem sap ABA concentration and stomatal conductance (reviewed in Dodd et al., 1996). When xylem sap was allowed to exude under root pressure alone, N-deprived plants showed increased xylem sap ABA concentrations (Goldbach et al., 1975; Krauss, 1978). However, this might be an artefact of the sap collection method. N deprivation decreases the exudation rate from detopped root systems (Kirkby and Armstrong, 1980; Chapin et al., 1988), while ABA concentration increases exponentially as the sap flow rate from the roots decreases (Else et al., 1995; Schurr and Schulze, 1995). Thus sap exuded from detopped root systems of N-deprived plants might be expected to show higher ABA concentrations. For this reason, sap was collected from excised whole shoots by pressurization. As far as is known, this is the first report of increased ABA concentration of xylem sap (Table 2) collected from N-deprived plants using this method.
The mechanism(s) causing this increased xylem sap ABA concentration is unknown. Although decreased leaf turgor is considered to trigger leaf ABA biosynthesis (Pierce and Raschke, 1980), this explanation is inconsistent with the increased shoot of N-deprived plants (Fig. 1b). Furthermore, N-deprived plants can show increased leaf ABA concentrations even when leaf turgor remains unchanged (Palmer et al., 1996). An increased xylem sap pH in response to N deprivation (Fig. 1c) might be expected to increase xylem ABA concentration as weak acids accumulate in alkaline compartments (Kaiser and Hartung, 1981). Alternatively, xylem sap contains an ABA precursor, which is hydrolysed at alkaline pH (Netting, 2000).
Although N deprivation increased xylem sap ABA concentration (Table 2), supplying 100 nM ABA via the xylem to detached N-deprived leaves did not statistically inhibit transpiration when the AX solution was at pH 7 (Fig. 3a, c), close to that observed in vivo (Fig. 1c). When the AX solution was at pH 6, 100 nM ABA induced a small (c. 20%) inhibition of transpiration of N-deprived leaves. Similarly, detached leaves of other dicotyledonous species such as Commelina communis (Trejo et al., 1993) and cotton (Radin et al., 1982) have shown minimal (<10%) inhibition of transpiration when supplied with 100 nM ABA via the transpiration stream. Presumably, mesophyll ABA catabolism prevents penetration of this ABA concentration to the guard cells (Trejo et al., 1993). N deprivation can increase stomatal sensitivity to ABA, but this was only detected when detached cotton leaves were fed ABA concentrations greater than 100 nM (Radin et al., 1982), and was not seen here with the lower ABA concentrations fed to Capsicum leaves (cf. Fig 3a, b and 3c, d). Thus increased xylem sap ABA concentration or an increased stomatal sensitivity to ABA did not appear to be responsible for stomatal closure of N-deprived Capsicum leaves.
Instead, the more alkaline xylem pH of N-deprived plants (Fig. 1c) could induce stomatal closure of detached leaves (Fig. 3), irrespective of the ABA concentration supplied. The similar pH response of root exudate and sap collected by shoot pressurization (Fig. 1c) suggests that xylem sap of N-deprived Capsicum plants is indeed more alkaline in vivo. Increased alkalinity of root exudate from N-deprived plants has been reported previously in Ricinus (Kirkby and Armstrong, 1980). This pH response is unlikely to be an artefact of the lower exudate flow rate of N-deprived plants, since xylem sap pH decreases when sap flow rate decreases in both Ricinus (Schurr and Schulze, 1995) and tomato (Else et al., 1995).
Mechanisms that increase xylem sap pH have been reviewed recently (Wilkinson and Davies, 2002). According to these authors, N deprivation in rapidly growing herbaceous species switches nitrate reduction to the roots (Lips, 1997). This produces hydroxyl ions which are converted to malate for transport to the shoot. Malate alkalizes xylem sap to a greater extent than nitrate. Measurement of root nitrate reductase activity and xylem sap organic acid concentrations following N deprivation would test this hypothesis.
Although increased xylem sap pH may initiate stomatal closure of N-deprived plants, the pH signal was transient and not seen on day 4 (Fig. 1c) although whole plant transpiration rates continued to decline (Fig. 1a). While this may suggest a greater role for changes in xylem sap ABA concentration, leaves detached from plants deprived of N for 4 d also showed no significant stomatal response to 100 nM ABA (data not shown). Detached N-deprived leaves showed a lower transpiration rate than N-supplied leaves even when fed an ‘optimal’ (pH 6, 10 nM ABA) AX solution (cf. Fig. 3c, d), suggesting either that the AX solution lacks a promoter of stomatal opening or that stomata were responding to factors residing within the leaf.
Exogenous cytokinins are known to promote stomatal opening (Incoll et al., 1990) and N deprivation decreases cytokinin supply from the roots (Sattelmacher and Marschner, 1978). Xylem sap from N–supplied Capsicum contains c. 5 nM zeatin riboside (C Ngo and IC Dodd, unpublished observations). However, supply of a 100-fold higher concentration of a synthetic cytokinin (which is presumably more resistant to catabolism) to N-deprived detached leaves was unable to restore transpiration rates to those of N-supplied leaves (Table 3). It seems likely that exogenous cytokinins can only promote stomatal opening when cytokinin metabolism is overwhelmed by supplying cytokinin concentrations many orders of magnitude greater than those found in planta (Radin et al., 1982; Stoll et al., 2000).
Sustained stomatal closure may also result from increased leaf ABA concentrations (Goldbach et al., 1975) or decreased leaf cytokinin concentrations (Sattelmacher and Marschner, 1978), although these variables were not measured here. However, stomatal closure of both ABA-deficient flacca and wild-type tomato following N deprivation (Chapin, 1990) tends to discount a role for increased leaf ABA concentrations in mediating stomatal closure under N deprivation. The stomatal responses of cytokinin-overproducing transgenics to N deprivation may provide further information.
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Withdrawal of N from the rhizosphere is an abrupt change, but this practice, prior to the harvest of hydroponically grown crops, has been suggested as a means of limiting nitrate losses to the environment (Le Bot et al., 2001). However, pronounced stomatal closure following N deprivation (Fig. 2) may limit photosynthesis, thus reducing the supply of assimilates to harvested crops. Understanding the mechanisms of stomatal closure following N deprivation may allow the design of ameliorating measures (e.g. foliar cytokinin spraying) to avoid stomatal closure in crops from which N has been withdrawn. During the early stages of N deprivation, stomatal closure is mediated by increases in xylem sap pH and ABA concentration. With prolonged N deprivation, stomatal closure is mediated by factors residing within N-deprived leaves.
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Acknowledgements |
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ICD thanks the Australian Research Council for financial support, Dr B Loveys (CSIRO Plant Industry, Adelaide) for the kind gift of [2H6] ABA and Dr J Ross (University of Tasmania) for GC-MS analysis. Mr W Bean is thanked for maintenance of the growth facilities.
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References |
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