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First published online September 17, 2004; 10.1104/pp.104.043844 Plant Physiology 136:3469-3477 (2004) © 2004 American Society of Plant Biologists
Bicarbonate-Induced Alkalinization of the Xylem Sap in Intact Maize Seedlings as Measured in Situ with a Novel Xylem pH Probe1Lehrstuhl für Biotechnologie, Biozentrum, Am Hubland, D–97074 Wurzburg, Germany
In higher plants the pH of the xylem sap plays an important role in drought signaling, growth regulation, and plant nutrition. However, the interpretation of the data is very controversial. The main reason for this is that the xylem pH in intact plants was not directly accessible hitherto. We present here a novel, minimally-invasive probe based on the xylem pressure-potential probe (used for measuring directly xylem pressure and the electrical potential between root xylem sap and medium). Single-tipped, double-barreled capillaries were used, one barrel served as H+-selective electrode, whereas pressure and electrical potential were recorded by the other one. Upon insertion of the probe into the root xylem of maize (Zea mays) seedlings, pH values ranging between about 4.2 and 4.9 were monitored when the roots were immersed in standard nutrient solution. The pH did not respond to changes in light irradiation (up to 300 µmol m–2 s–1), but increased upon exposure of the root to 5 or 20 mM bicarbonate in the bath solution. Changes in pH could also be recorded in transpiring plants when the root was cut below the insertion point of the probe and placed in media with different pH. The data support the hypothesis of Mengel ([1994] Plant Soil 165: 275–283) that upon external supply with bicarbonate Fe is immobilized in the leaf apoplast via changes in xylem pH.
Changes in the pH of the xylem sap have been associated with various aspects of plant (stress) physiology. Evidence has been presented for a crucial role of xylem pH in growth regulation (Mizuno and Katou, 1991  ), in plant response to waterlogging (Jackson et al., 2003), and in adjusting plant water relations under conditions of drought stress (Wilkinson and Davies, 1997; Wilkinson, 1999; Zwieniecki et al., 2001), e.g. by a mobilization of abscisic acid that regulates stomatal aperture (MacRobbie, 1998). However, its putative involvement in the so-called lime chlorosis phenomenon, i.e. (local) leaf yellowing that is observed with plants growing on carbonate-rich soils (Mengel, 1994), appears to stand on less solid ground. Chlorosis is a symptom of cellular Fe deficiency that results from a limited availability of apoplastic Fe in the leaf. It is apparently not necessarily associated with a decrease in Fe uptake by the roots. An elevated bicarbonate concentration of the soil has been identified as a major factor for the induction of lime chlorosis in various crop species including maize (Zea mays; Marschner, 1995; Alhendawi et al., 1997). In calcareous soils bicarbonate concentrations are usually in the range between 1 and 5 mM, but can readily rise to values of 10 mM and higher, particularly under waterlogging conditions (McCray and Matocha, 1992). Mengel et al. (1994) hypothesized that bicarbonate-induced chlorosis is caused by transport of bicarbonate into the stele that leads to an alkalinization of the xylem sap and, in turn, of the leaf apoplast. Symptoms of Fe deficiency develop at a high apoplastic pH due to a repression of FeIII reduction, which is a prerequisite for Fe uptake by mesophyll cells. Several authors have tested Mengel's hypothesis by measuring the effect of bicarbonate on xylem sap pH, but no final conclusion was reached. Alhendawi et al. (1997) observed a moderate pH increase from 5.18 to 5.65 when maize roots were exposed to 20 mM bicarbonate, but no significant increase was observed at concentrations of 10 mM or below; these authors concluded that xylem or apoplastic pH changes were of no major importance for lime chlorosis. For sunflower, Mengel et al. (1994) reported an increase in the leaf xylem pH by 0.8 units after perfusion of the leaves with solutions that contained HCO3–, but Nikolic and Römheld (1999, 2002) and Kosegarten et al. (2001) found no effect on the xylem pH for this species when bicarbonate (up to 50 mM) was supplied to the roots. In sugar beet even a slight decrease in xylem sap pH was observed (Lopez-Millan et al., 2000) upon exposure of the roots to low bicarbonate concentrations. These discrepancies cannot be explained by differences in the experimental setup or by variations among species alone, especially since the crop plants used in these studies were highly susceptible to lime chlorosis. Rather, problems may arise from the use of inadequate methods for assessing the xylem sap pH in the intact plant (Yu et al., 2000). Xylem sap was obtained by using root pressure exudation after decapitation of the shoot (Alhendawi et al., 1997; Nikolic and Römheld, 1999, 2002), or apoplastic fluid was collected by employing centrifugation methods (Nikolic and Römheld, 1999; Lopez-Millan et al., 2000). Rowan et al. (2000) have recently demonstrated that root pressure exudate does not exclusively originate from the xylem sap. Moreover, ion and water relations of decapitated plants are hardly comparable with the situation in the intact transpiring organism (for a detailed discussion, see Schurr, 1998). Collection of apoplastic fluid by centrifugation is also susceptible to artefacts (Sattelmacher, 2001). Mengel et al. (1994) employed a method for in situ recording of pH in the leaf apoplast using fluorescein isothiocyanate (FITC) dextran, but the composition of the apoplastic fluid may have been altered when the dye was loaded by infiltration of the leaf. Hence, it still remains unclear whether this method properly reflects leaf apoplastic pH in the intact plant. In the future, progress may come from transgenic "self-reporting" Arabidopsis plants that express pH indicators in the apoplast (Gao et al., 2004).
In this study, the effect of externally applied bicarbonate on xylem sap pH in the root was investigated using a novel, minimally-invasive technique that allows for continuous, in situ recording of the xylem pH on intact plants. A pH-selective xylem probe was designed in analogy to the multifunctional xylem K+ probe (Wegner and Zimmermann, 2002
Calibration of the Xylem pH Probe
A schematic representation of the probe is shown in Figure 1 (see also "Materials and Methods" for a detailed description). The integrated pH electrode was always calibrated before the tip of the probe was inserted into the root tissue and again after withdrawal at the end of the experiment. To this end, the probe tip was successively exposed to a series of calibration media adjusted to pH values ranging from 4.0 to 7.0, and the electrical potential drop across the H+-selective matrix was recorded with respect to a reference electrode. A typical trace showing the H+ electrode potential during the calibration procedure is depicted in Figure 2A. During medium exchange the electrode tip was briefly exposed to air, leading to an interruption of the electrical circuit and an immediate clipping of the voltage signal (arrows). A calibration curve was generated by plotting steady-state electrical potentials against the corresponding pH values of the calibration media (Fig. 2B). A linear relationship was observed between electrode potential and pH in the range tested here with a slope of –53 mV/pH unit. It is important to note that good agreement was found between potentials recorded before insertion of the electrode into root tissue and after subsequent withdrawal (black and white symbols, respectively). Generally, an electrode was discarded when the results of pre- and recalibration deviated significantly. In this case, the data of the particular experiment were not included in the analysis. Before use in physiological studies, the selectivity of pH electrodes had been tested by recording the H+ electrode potential after addition of various salts to the calibration medium that could possibly interfere with the pH measurement in the xylem (Schurr and Schulze, 1995
Xylem Sap pH Remains Unaffected by the Light Regime When the Root Is Immersed in Standard Medium
The feasibility of the new probe technique for simultaneous recording of xylem sap pH, TRP, and xylem pressure was tested on seminal roots of maize seedlings. In the first set of experiments, the response of these parameters to a varying light regime was tested. A typical experiment is shown in Figure 3. The probe was inserted at the root base 1.3 cm away from the caryopsis at laboratory light (10 µmol m–2 s–1). Upon puncturing of a vessel, the pressure dropped within seconds to a subatmospheric value as observed previously (Balling and Zimmermann, 1990
Xylem pH Recordings on Perfused Xylem Vessels
The xylem pressure and TRP changes observed upon light irradiation were comparable to those observed previously with the unmodified xylem pressure-potential probe, suggesting proper functioning of the xylem pH probe. This conclusion was further supported by measurements in which the root xylem was perfused with artificial media adjusted to various pH values for in situ calibration of the probe. To this end, the probe was inserted into a root xylem vessel at a photon density of 300 µmol m–2 s–1. When stable values for xylem pH, xylem pressure, and TRP were recorded, the root was cut 0.5 to 1 cm below the site of impalement (i.e. in upstream direction). Via the cut surface of the root stump that remained attached to the transpiring shoot, bath solution was sucked into the open xylem vessels, including the one that had been punctured by the probe. Recordings obtained during one out of three experiments of this type are depicted in Figure 4A. Xylem pressure was about –0.07 MPa in the intact root. Upon cutting, it rapidly relaxed to atmosphere (half time 6.2 s). As expected, upon xylem perfusion with the bath solution (pH 5.5) the pH increased from 4.8 to 5.4. When the bath pH was then elevated to 6.0, the pH registered by the probe promptly rose to 6.1 and subsequently relaxed to 5.8. Acidification of the bath to 4.5 and subsequent increase to 5.0 were also reflected by the probe recordings (final values 4.6 and 4.9, respectively), but with some delay. For clarity, the TRP is not shown in Figure 4A. A plot of the steady-state pH values registered by the probe versus the pH of the perfusate (Fig. 4B) for this and two other experiments showed good agreement between the data. The outcome was not affected by the sequence of the imposed pH changes. Slight deviations of the measured pH values from those adjusted in the perfusate may be due to the activity of proton pumps in stelar cells (De Boer and Prins, 1985
Supplying Maize Roots with Bicarbonate Leads to an Alkalinization of the Xylem Sap
The effect of bicarbonate on xylem sap pH, TRP, and xylem pressure in seminal roots of maize seedlings was studied by monitoring these parameters with a xylem pH probe prior to and after the addition of 20 or 5 mM NaHCO3, respectively, to the bath. Direct effects of bicarbonate could be separated from indirect effects related to changes in osmotic pressure and bath pH by performing the experiment in two steps. At the beginning, the probed root was immersed in standard bath medium; then the ambient pH was raised to 8.0 by addition of NaOH and the final osmotic pressure was adjusted with mannitol1; subsequently, bicarbonate was supplied isoosmotically at a constant pH. It should be noted that changes in the concentrations of mannitol and Na+ did not affect xylem sap pH. This was verfied by a separate experiment with the xylem pH probe in which mannitol was replaced isoosmotically by NaCl (data not shown). A bath pH of 8.0 was selected to prevent removal of HCO3– from the solution by formation of CO2 (or by precipitation of CaCO3). It should be noted that this pH is not uncommon for calcareous soils where lime chlorosis usually occurs. Typical experiments demonstrating the effect of 20 and 5 mM NaHCO3 at an ambient pH of 8.0 are depicted in Figure 5, A and B, respectively. In Figure 5A, the osmolality was increased from 26 mosmol kg–1 in standard medium to 71 mosmol kg–1 at t = 52 min, evoking a xylem pressure decrease by 0.019 MPa (from 0.069–0.050 MPa) and a transient hyperpolarization of the xylem by –10 mV from a steady-state TRP of –13 mV in standard medium. Together with the osmotic pressure increase, the pH in the bath was elevated from 5.5 to 8.0. This led to an increase in xylem sap pH by more than 1 unit (from 4.0 to 5.23). The concomitant change in the osmotic pressure of the bath did not affect xylem sap pH; this was tested in separate experiments (data not shown). Subsequent isoosmotic addition of 20 mM NaHCO3 at a constant ambient pH (8.0) resulted in a further xylem pH increase by 1.48 units to a final value of 6.71; alkalinization started after a short lag time of about 3 min. Bicarbonate also induced a rapid hyperpolarization of the TRP by –26 mV that was partly reversed later on. The xylem pressure was hardly affected; it decreased slightly from 0.050 to 0.038 MPa during the presence of NaHCO3 in the bath. At t = 182 min, photon density was increased from about 10 to 300 µmol m–2 s–1 in order to test the response of xylem pressure to an increase in light irradiation. Pressure dropped to values below vacuum after a lag time of 3 min, indicating propper insertion of the probe in a xylem vessel. The experiment was terminated by withdrawing the probe. Prior to the response of the xylem pressure, the TRP went more negative by –11 mV. Interestingly, the xylem pH decreased in the presence of bicarbonate when the plant was exposed to a higher photon density. Qualitatively similar results were obtained when a root was supplied with 5 mM NaHCO3 (Fig. 5B; only the response to bicarbonate is shown), but the change in xylem sap pH was less pronounced (here by 0.50 units, i.e. from 5.52–6.02). Again, the pH responded after a lag time of almost 5 min. Interestingly, 5 mM bicarbonate induced only a small, transient hyperpolarization of the TRP (by –6 mV). In this experiment, xylem pressure had already dropped below vacuum at the low photon density (10 µmol m–2 s–1) indicating that the measurement was technically sound and additional testing of the pressure response to light was not required. Differences in xylem pressure like those occurring between the experiments shown in Figure 5, A and B reflect the usual range of variability (Schneider et al., 1997a
The effect of bicarbonate on xylem sap pH (or H+ activity) and on the TRP is summarized in Figure 5, C and D, respectively. Alkalinization of the xylem ranged from 0.50 to 0.63 pH units upon addition of 5 mM bicarbonate (n = 3; mean pH difference, 0.59 units) and from 0.88 to 1.54 units upon addition of 20 mM bicarbonate (n = 5; mean pH difference, 1.07 units). Five minutes after bicarbonate addition TRP had changed on average by –5 mV (5 mM NaHCO3) and by –15 mV (20 mM), respectively. Interestingly, in some experiments (as the one shown in Fig. 5A) an alkalinization of the bath (from 5.5–8.0) upon NaOH addition induced an increase in the xylem pH by more than 1 unit. However, the response was quite variable. In one experiment the xylem pH was not affected at all and in three other experiments alkalinization was less pronounced (less than 0.5 units). These discrepancies can be explained with individual differences in lateral root formation among the seminal roots of the maize seedlings that had been selected for these experiments. At the lateral root primordia the endodermis is discontinuous, thus leakage of solutes into and out of the stele can occur at these sites via an apoplastic pathway (Steudle et al., 1993 ).
The xylem pH probe presented in this communication is a new tool to assess the multiple roles of xylem sap pH in plant (stress) physiology. In contrast to conventional techniques used to measure this parameter, the minimally invasive probe allows for continuous in situ monitoring of xylem pH (together with the TRP and xylem pressure) on intact, transpiring plants. In this study we have provided strong evidence (Figs. 2–4  ) that the xylem pH probe reflects the correct values for xylem pH as well as for the TRP and xylem pressure in the intact plant. Pressure and electrical data were in agreement with previous reports on young maize seedlings (Schneider et al., 1997a, 1997b; Wegner and Zimmermann, 1998, 2002; Zimmermann et al., 2002, 2004), and pH measurements could be verified with an in situ calibration procedure (Fig. 4), demonstrating proper functioning of the probe. Xylem pH changes imposed in these experiments by vessel perfusion were comparable to those occurring in the intact plant or even exceeded them. Mean pH values measured in roots of intact maize seedlings ranged between about 4.38 at low light irradiation and 4.85 after long-term exposure to a photon density of 300 µmol m–2 s–1. Both data sets were not significantly different, but further testing with stronger light sources is required to assess effects of prolonged illumination on xylem pH. However, at both levels of irradiation applied in this study mean pH values differed significantly from those usually measured both in the cytoplasm and the vacuole of root cells (Walker et al., 1995). This finding adds to the bulk of evidence indicating that xylem probes are properly inserted into the lumen of fully differentiated xylem vessels (Wegner and Zimmermann, 2002; Zimmermann et al., 2004). In view of the low pH values measured with the xylem pH probe, it is also very unlikely that the xylem sap in the punctured vessel is contaminated by permanent leakage of cell contents, which are expected to be more alkaline. This is also supported by the apparent lack of sensitivity of the xylem pH to a varying light regime in the range tested in this study. Substances leaking into the punctured vessel would have a strong impact on local xylem pH at low light irradiation (corresponding to a low flow rate; Kuchenbrod et al., 1996), but would be diluted and rapidly swept away at the higher photon density when the flow rate increased. This would be reflected by a change in xylem pH as measured with the probe. However, the pH remained invariant to short-term changes in light intensity, indicating that few—if any—buffering compounds were released at the site of impalement.
The pH values obtained with the probe are also somewhat lower than those measured in xylem sap collected from severed maize roots under similar experimental conditions, probably due to the use of gross, massive invasive techniques in those studies. Davis and Higinbotham (1969)
Previous failure to demonstrate the effect of bicarbonate on xylem sap pH (except for Mengel et al., 1994
Our data indicate that bicarbonate is transported radially into the root stele, in agreement with Mengel's hypothesis (Mengel, 1994
In summary, the novel pH probe introduced in this communication paves the way to analyze the physiological processes that induce lime chlorosis in various crop species growing on calcareous soils, as well as other aspects of plant nutrition that involve changes in xylem sap pH. The data presented here lend strong support to Mengel's hypothesis (Mengel, 1994 ) that bicarbonate is transported radially into the root stele and subsequently into the leaves leading to an increase in apoplastic pH; additional alkalinization may come from bicarbonate uptake by bundle sheath cells via a symport with protons, as suggested previously for mesophyll cells of various C3 species by Savchenko et al. (2000). It is generally accepted that an alkalinization of the leaf apoplast would inhibit reduction of FeIII to FeII and thus hamper Fe uptake by the cells (Mengel et al., 1994; Nikolic and Römheld, 1999, 2002); it may also be relevant for Zn nutrition (Pearce et al., 1999). Rigorous testing of these hypotheses requires further experimentation with the xylem pH probe on leaves, e.g. comparing xylem pH at green and chlorotic sites.
Plant Material
Maize seedlings (Zea mays L. cv Bangui) were cultured on hydroponics as described previously (Wegner and Zimmermann, 1998
The pH-sensing xylem pressure-potential probe, briefly termed xylem pH probe in this communication, is sketched in Figure 1. It was designed by analogy to the xylem K+ probe published previously (Wegner and Zimmermann, 2002
For recording of xylem pH double-barreled microcapillaries were fabricated as described elsewhere (Wegner and Zimmermann, 2002
The xylem pressure-potential probe used here has been described in detail elsewhere (Wegner and Zimmermann, 2002 The ready-to-use probe was mounted on a micromanipulator, and an Ag/AgCl electrode was introduced into the ion-selective barrel. Electrical potentials were measured with a high-impedance electrometer (FD 223, WPI, Sarasota, FL).
Seminal roots of intact seedlings were fixed on a perspex holder and immersed in standard bath medium composed as follows (in mM): 1 KCl, 2 MgCl2, 2 CaCl2, 10 MES adjusted to pH 5.5 with BTP. The osmolality was cryoscopically determined to be 26 mosmol kg–1 (Osmomat 030-M, Gonotech GmbH, Berlin). Before the xylem pH probe was inserted into the root (usually at the root base 1–5 cm away from the caryopsis) the integrated pH electrode was calibrated with media containing 0.1 or 1 mM KCl and 10 mM MES; the pH had been adjusted to values ranging from 4.0 to 7.0 with BTP using a glass electrode (E512, Metrohm, Herisau, Switzerland). The values were checked with a digital pH meter (KS723, Shindengen, Hong Kong, China), that had been calibrated independently. The impalement procedure that required some precautions has been described in detail elsewhere (Balling and Zimmermann, 1990
Data acquisition has been described in detail previously (Wegner and Zimmermann, 2002 Statistical calculations were performed on H+ concentrations since there is no mathematical basis for the computation of arithmetic means and SDs of pH values (which represent –log [H+]). When average pH values are given, they were obtained by recalculation from the respective mean H+ concentrations. Differences between mean values were tested for significance using Student's t test (significance level P = 0.05). Received March 31, 2004; returned for revision May 18, 2004; accepted May 23, 2004.
1 This work was supported by the Deutsche Forschungsgemeinschaft (grant no. We2766/1–1 to L.H.W.)  www.plantphysiol.org/cgi/doi/10.1104/pp.104.043844. * Corresponding author; e-mail lars.wegner{at}biozentrum.uni-wuerzburg.de; fax 49–931–8884509.
Alhendawi RA, Römheld V, Kirkby EA, Marschner H (1997) Influence of increasing bicarbonate concentrations on plant growth, organic acid accumulation in roots and iron uptake by barley, sorghum, and maize. J Plant Nutr 20: 1731–1753 Ammann D (1986) Ion-Selective Microelectrodes. Springer, Berlin Balling A, Zimmermann U (1990) Comparative measurements of the xylem pressure of Nicotiana plants by means of the pressure bomb and pressure probe. Planta 182: 325–338[CrossRef][ISI]
Chang K, Roberts JKM (1992) Quantitation of rates of transport metabolic fluxes and cytoplasmic levels of inorganic carbon in maize root tips during potassium ion uptake. Plant Physiol 99: 291–297 Davis RF, Higinbotham N (1969) Effects of external cations and respiratory inhibitors on electrical potential of the xylem exudate of excised corn roots. Plant Physiol 44: 1382–1392 De Boer AH, Prins HBA (1985) Xylem perfusion of tap root segments of Plantago maritima: the physiological significance of electrogenic xylem pumps. Plant Cell Environ 8: 579–586[CrossRef] Engels C (1999) Regulation of xylem transport of calcium from root to shoot of maize by growth-related demand. J Plant Nutr Soil Sci 162: 287–294
Felle H (1998) The apoplast pH of the Zea mays root cortex as measured with pH-sensitive microelectrodes: aspects of regulation. J Exp Bot 49: 987–995 Felle H, Bertl A (1986) The fabrication of H+-selective liquid-membrane microelectrodes for use in plant cells. J Exp Bot 37: 1426–1428 Frommer WB, von Wiren N (2002) Ping-pong with boron. Nature 410: 282–283
Gao D, Knight MR, Trewavas AJ, Sattelmacher B, Plieth C (2004) Self-reporting Arabidopsis expressing pH and [Ca2+] indicators unveil ion dynamics in the cytoplasm and in the apoplast under abiotic stress. Plant Physiol 134: 898–908 Jackson MB, Saker LR, Crisp CM, Else MA, Janowiak F (2003) Ionic and pH signalling from roots to shoots of flooded tomato plants in relation to stomatal closure. Plant Soil 253: 103–113[CrossRef]
Köhler B, Raschke K (2000) The delivery of salts to the xylem: three types of anion conductance in the plasmalemma of the xylem parenchyma of roots of Hordeum vulgare L. Plant Physiol 122: 243–254 Köhler B, Wegner LH, Osipov V, Raschke K (2002) Loading of nitrate into the xylem: apoplastic nitrate controls the voltage dependence of X-QUAC, the main anion conductance in xylem-parenchyma cells of barley roots. Plant J 30: 133–142[CrossRef][ISI][Medline] Kosegarten H, Hoffmann B, Mengel K (2001) The paramount influence of nitrate in increasing apoplastic pH of young sunflower leaves to induce Fe deficiency chlorosis, and the re-greening effect brought about by acidic foliar sprays. J Plant Nutr Soil Sci 164: 155–163[CrossRef] Kuchenbrod E, Landeck M, Thürmer F, Haase A, Zimmermann U (1996) Measurement of water flow in the xylem vessels of intact maize plants using flow-sensitive NMR imaging. Bot Acta 109: 184–186
Lopez-Millan AF, Morales F, Abadia A, Abadia J (2000) Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiol 124: 873–884 MacRobbie EAC (1998) Signal transduction and ion channels in guard cells. Philos Trans R Soc Lond B Biol Sci 353: 1475–1488[CrossRef][ISI][Medline] Marschner H (1995) Mineral Nutrition of Higher Plants. Academic Press, London, San Diego McCray JM, Matocha JE (1992) Effects of soil water levels on solution bicarbonate, chlorosis and growth of sorghum. J Plant Nutr 15: 1877–1890 Mengel K (1994) Iron availability in plants tissues: iron chlorosis on calcareous soils. Plant Soil 165: 275–283[CrossRef] Mengel K, Plänker R, Hoffmann B (1994) Relationship between leaf apoplast pH and iron chlorosis of sunflower (Helianthus annuus L). J Plant Nutr 17: 1053–1065
Miller DM (1985) Studies of root function in Zea mays. III. Xylem sap composition at maximum root pressure provides evidence of active transport into the xylem and a measurement of the reflection coefficient of the root. Plant Physiol 77: 162–167
Mizuno A, Katou K (1991) The characteristics of the adjustment in the pH of the xylem exudate of segments of Vigna hypocotyls during xylem perfusion. Plant Cell Physiol 32: 403–408 Nikolic M, Römheld V (1999) Mechanism of Fe uptake by the leaf symplast: Is Fe inactivation in a leaf a cause of Fe deficiency chlorosis? Plant Soil 215: 229–237[CrossRef] Nikolic M, Römheld V (2002) Does high bicarbonate supply to roots change availability of iron in the leaf apoplast? Plant Soil 241: 67–74[CrossRef] Pearce RC, Li Y, Bush LP (1999) Calcium and bicarbonate effects on the growth and nutrient uptake of barley tobacco seedlings: hydroponic culture. J Plant Nutr 22: 1069–1078 Romero MF, Hediger MA, Boulpaep EL, Boron WF (1997) Expression cloning and characterization of a renal electrogenic Na+/HCO3– cotransporter. Nature 387: 409–413[CrossRef][Medline] Rowan A, McCully ME, Canny MJ (2000) The origin of the exudate from cut maize roots. Plant Physiol Biochem 38: 957–967[CrossRef] Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytol 149: 167–192[CrossRef] Savchenko G, Wiese C, Neimanis S, Hedrich R, Heber U (2000) PH regulation in apoplastic and cytoplasmic cell compartments of leaves. Planta 211: 246–255[CrossRef][ISI][Medline] Schneider H, Wistuba N, Miller B, Geßner P, Thürmer F, Melcher P, Meinzer F, Zimmermann U (1997a) Diurnal variation in the radial reflection coefficient of intact maize roots determined with the xylem pressure probe. J Exp Bot 48: 2045–2053 Schneider H, Zhu JJ, Zimmermann U (1997b) Xylem and cell turgor pressure measurements in intact roots of glycophytes: transpiration induces a change in the radial and cellular reflection coefficients. Plant Cell Environ 20: 221–229 Schurr U (1998) Xylem sap sampling: new approaches to an old topic. Trends Plant Sci 3: 293–298 Schurr U, Schulze E-D (1995) The concentration of xylem sap constituents in root exudate, and in sap from intact, transpiring castor bean plants (Ricinus communis L.). Plant Cell Environ 18: 409–420 Steudle E, Murrmann M, Peterson CA (1993) Transport of water and solutes across maize roots modified by puncturing the endodermis. Plant Physiol 103: 335–349[Abstract] Takano J, Nogushi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420: 337–340[CrossRef][Medline] Walker DJ, Leigh RA, Miller AJ (1995) Potassium homeostasis in vacuolate plant cells. Proc Natl Acad Sci USA 93: 10510–10514 Wegner LH, Raschke K (1994) Ion channels in the xylem parenchyma of barley roots: a procedure to isolate protoplasts from this tissue and a patch-clamp exploration of salt passageways into xylem vessels. Plant Physiol 105: 799–813[Abstract] Wegner LH, Sattelmacher B, Läuchli A, Zimmermann U (1999) Trans-root potential, xylem pressure, and root cortical membrane potential as influenced by nitrate and ammonium. Plant Cell Environ 22: 1549–1558[CrossRef] Wegner LH, Zimmermann U (1998) Simultaneous recording of xylem pressure and trans-root potential in roots of intact glycophytes using a novel xylem pressure probe technique. Plant Cell Environ 21: 849–865[CrossRef] Wegner LH, Zimmermann U (2002) On-line measurements of K+ activity in the tensile water of the xylem conduit of higher plants. Plant J 32: 409–417[CrossRef][ISI][Medline] Wilkinson S, Davies WJ (1997) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Physiol 113: 559–573[Abstract] Wilkinson S (1999) PH as a stress signal. Plant Growth Regul 29: 87–99 Yu Q, Tang C, Kuo J (2000) A critical review on methods to measure apoplastic pH in plants. Plant Soil 219: 29–40[CrossRef] Zimmermann U, Schneider H, Thürmer F, Wegner LH (2002) Pressure probe measurements of the driving forces for water transport in intact higher plants: effects of transpiration and salinity. In A Läuchli, U Lüttge, eds, Salinity: Environment–Plants–Molecules. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 249–270 Zimmermann U, Schneider H, Wegner LH, Haase A (2004) Tansley Review: Water ascent in tall trees: Does evolution of land plants rely on a highly metastable state? New Phytol 162: 575–615[CrossRef]
Zwieniecki MA, Melcher P, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291: 1059–1062
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