JXB Advance Access originally published online on February 7, 2005
Journal of Experimental Botany 2005 56(413):879-886; doi:10.1093/jxb/eri080
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RESEARCH PAPER |
Radial transport of water and abscisic acid (ABA) in roots of Zea mays under conditions of nutrient deficiency
1Julius-von-Sachs-Institut für Biowissenschaften, Universität Würzburg, Julius-von-Sachs-Platz 2, D-97082 Würzburg, Germany
2Interdiszipliäres Ökologisches Zentrum, TU Bergakademie, Freiberg, Leipziger Str. 29, D-09599 Freiberg, Germany
* To whom correspondence should be addressed. Fax: +49 931 888 6158. E-mail: hartung{at}botanik.uni-wuerzburg.de
Received 13 July 2004; Accepted 18 November 2004
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Abstract |
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Radial water (JV) and abscisic acid (ABA) flows (JABA) through maize root seedlings have been investigated under different conditions of nutrient deficiency. Whereas JV was reduced under nitrogen deficiency, potassium deficiency stimulated JV. A substantial increase of JABA was observed in roots kept under potassium deficiency. The observed changes of JV might have resulted from changed barrier properties of the endodermis. Nitrogen and potassium deficiency also caused an accumulation of endogenous ABA in root tissues. Under all conditions studied, except under K+-deficiency, external ABA (100 nM) caused an increase of JV. The data of this study were used to analyse the relations between internal and endogenous root ABA, JV, and JABA. The internal ABA of root tissues was positively correlated with JV and was highly significant (P <0.001 for internal and P=0.03 for endogenous root ABA) within the range 2–300 pmol g–1 FW. It was also highly positively correlated to the radial ABA flows. There was also a highly positive correlation between JV and JABA. The data of this study indicate, for the first time, the relations between internal ABA, water, and ABA flows. Independent of treatment with external ABA, an ABA transport by solvent drag across the endodermis is confirmed.
Key words: Abscisic acid, nutrient deficiency, radial water transport
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Abscisic acid (ABA) functions as a plant stress hormone in both leaves (where it regulates stomatal conductance) and roots where its effects are less well researched. Within roots ABA can increase the hydraulic conductivity (Lpr) of the cortical root cells resulting in improved water uptake under conditions of mild water shortage (Hose et al., 2000
; Wan et al., 2004). An involvement of aquaporins in the stimulation of the water flow (JV) and Lpr has been suggested. Wan et al. (2004) concluded that ABA may stabilize aquaporins in plasma membranes and may avert their collapse during the passage of water through the pores. This mechanism seems to be important when water passes the pores with a high velocity. Others have suggested that ABA-dependent gene expression of aquaporins could play an important role in regulating aquaporin density/frequency and root Lp (Kaldenhoff et al., 1996, 1998). However, studies with transgenic plants that exhibit either low or high amounts of aquaporins did not support this idea (Hose, 2000). The regulation of aquaporins by phosphorylation has not been conclusively demonstrated in roots.
In addition to the above considerations, ABA has been shown to be the most important long-distance stress signal produced by the roots as the soil is drying and it is transported in the xylem to the shoot where, as indicated above, guard cells and meristems are affected. Two processes modulate the intensity of the ABA signal in the xylem sap, biosynthesis and lateral transport from the cortex to the xylem vessels. Since the latter involves significant transport in the apoplast, the Casparian bands in the endodermis and the hypodermis, being the major transport barriers in the root, control the intensity of the transport signal. Freundl et al. (1998) and Schraut et al. (2004) demonstrated that ABA is transported directly across the Casparian bands of the endodermis in maize roots to a significant extent, with the water flow by solvent drag. The exodermis proved to be a more effective barrier which can reduce both influx and efflux of external ABA (Hose et al., 2001).
Soils of extreme habitats are often alkaline, or loaded with large amounts of sodium chloride, or deficient in the major nutrients. Nutrient shortage was reported to stimulate ABA biosynthesis in roots and to intensify the root-to-shoot ABA signal (Chapin, 1990; Peuke et al., 1994; a detailed list of references about the relations between ABA synthesis and nitrogen deficiency is given here; phosphate deficiency, Jeschke et al., 1997; Jeschke and Hartung, 2000; potassium deficiency, Peuke et al., 2002). Nitrogen, phosphorus, and sulphur deficiencies were shown to reduce the hydraulic conductivity of roots (Radin and Matthews, 1989; Karmoker et al., 1991; Barthes et al., 1995; Carvajal et al., 1996; Reinbott and Blevins, 1999; Clarkson et al., 2000). By contrast, water flows and hydraulic conductivity (Lpr) of sunflower roots increased under conditions of potassium starvation (Quintero et al., 1998). Equally, Radin and Matthews (1989) concluded that in phosphorus-deficient cotton roots the apoplastic bypass flow of water was increased. Thus the results on the physiological relationships between nutrient supply, ABA biosynthesis and accumulation in roots, radial ABA and water flow through roots, and thus the intensity of the ABA-signal in the xylem are controversial. One reason for these conflicting reports may be the application of exogenous ABA without knowledge of tissue ABA concentrations. Therefore in this study, for the first time, the relations between the internal root ABA concentration, JABA, and JV under different conditions of nutrient deficiency, as well as the internal ABA distribution in the root hair zone of maize roots, have been studied to elucidate further the role of ABA under conditions that might occur in soils of extreme habitats.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Plant material
Seeds of maize (Zea mays L. cv. Helix, Kleinwanzlebener Saatzucht AG, Einbeck, Germany) were germinated on filter paper soaked with 0.5 mM CaSO4 for 4 d at 26 °C in the dark. Seedlings were transferred to aerated hydroponic culture and kept in a greenhouse with an additional light source (mercury vapour lamp, 200 µmol m–2 s–1; day/night 16/8 h, 25/17 °C) for 7 d. The standard nutrient solution contained following nutrients: 1.5 mM KH2PO4, 2.0 mM KNO3, 1.0 mM CaCl2, 1.0 mM MgSO4, and 18 µM FeNaEDTA, 8.1 µM H3BO3, 1.5 µM MnCl2 at pH 5.5. For nutrient-deficiency experiments, caryopses were removed before transplanting in hydroponic culture to avoid interference with the endogenous nutrients of the caryopsis. The standard nutrient solution was modified by replacing the corresponding ion as shown below. KNO3 was replaced by KCl in the case of
deficiency, KH2PO4 by KCl in the case of 
deficiency, MgSO4 by MgCl2 in the case of 
deficiency, and K+ by Na+ in the case of K+ deficiency. For conditions of Ca2+ deficiency, CaCl2 was removed. In addition, plants were cultivated in total nutrient-deficient conditions supplied with 0.5 mM CaSO4 only. Thus the period of starvation was 7 d in all cases. When seedlings have been cultivated without their caryopses in some of the experiments 5 mM glucose and 100 units penicillin G (benzylpenicillin, Sigma-Aldrich, Taufkirchen, Germany) were added to the nutrient medium 24 h before starting the experiment.
Determination of water-flow (JV)
Excised primary root systems, with the mesocotyl still attached, were fixed to a capillary using a pressure-tight silicon seal fixed by a screw (Freundl et al., 1998). Roots were stored in an aerated darkened pot containing the same medium that the plants were cultivated in. Suction of –0.06 MPa applied to the root system caused xylem sap flow into a calibrated capillary. After 20 min the flow of water across the root system was steady. The water flow was determined by harvesting and weighing the xylem sap samples at 10 min intervals. (±) Abscisic acid (Sigma-Aldrich, Taufkirchen, Germany, final concentration of 100 nM (+) ABA) was added to the medium 60 min after the beginning of the experiment and xylem sap was harvested for another 120 min. Water flow JV (m3 m–2 s–1) was calculated for the period before and after the addition of ABA interval using the volume of the collected sap related to the surface area of the root system and time. An image analysing system based on a scanning system (scanwise 1.2.0.5
[EC]
., Agfa) and software (WinRHIZO Pro V. 2002b, Regent Instruments Inc.) was used to determine root surface areas. The measurements were performed as described earlier by Freundl et al. (1998).
It should be noted that the effects of nutrient starvation described later were particularly clear from April to July. Later in the year they were less distinct. If not otherwise stated data are therefore taken from that period.
Analysis of ABA
Tissue samples were frozen immediately after the experiment in liquid nitrogen and extracted by 80% methanol at –18 °C. The extract was passed through a SEP-Pak C18-cartridge (Waters, Eschborn, Germany) and eluted with 1 ml 80% methanol. After removal of the methanol of the combined eluates under reduced pressure, the pH of the aqueous fraction was adjusted to 3.0 and partitioned three times against ethyl acetate at pH 3. The combined organic fractions were evaporated to dryness and redissolved in TBS-buffer (TRIS-buffered saline; 150 mmol l–1 NaCl, 1 mmol l–1 MgCl2 and 50 mmol l–1 TRIS; pH 7.8). Xylem sap samples were diluted in TBS-buffer without further purification. Both were analysed for free ABA by an immunological ABA assay (ELISA) (Mertens et al., 1985; Peuke et al., 1994). The amounts of ABA in the xylem sap samples were used to calculate the radial ABA flow JABA (mol m–2 s–1) as described by Freundl et al. (1998).
Immunolocalization of ABA
For immunolocalization, seedlings of Zea mays were used that had been cultivated as for ABA flow measurements. Samples have been prepared as described in Schraut et al. (2004). A hydrostatic pressure gradient of –0.06 MPa was applied to the cut surface of excised root systems to induce a radial water flow. ABA (100 nM) was added to the external medium. After 40 min root segments above the root hair zone were fixed immediately with 3% paraformaldehyde in 4% 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide (EDAC) under reduced pressure to immobilize ABA. Immunolocalization has been performed as described previously (Veselov et al., 2002; Langhans et al., 2001; Schraut et al., 2004) using specific monoclonal ABA-antibody (ABA-15-I-c-5; Agdia/Linaris, Wertheim-Bettingen, Germany) and the red Alexa flour conjugate 568 (568 goat anti-mouse IgG, H+L, Molecular Probes, Göttingen, Germany) as a secondary antibody. Sections were stained with toluidine blue to quench the autofluorescence of the lignified cell walls in the root tissue and viewed with a confocal laser scanning microscope (CLSM) (Zeiss LSM 5 Pascal 5; Axioskop 2 mot plus; excitation 543, HFT 543, NFT 635, emission (BP) 560–615). Pictures were converted to the glow mode to improve contrasts. A series of controls have been investigated routinely to confirm the reliability of the technique, as described previously by Schraut et al. (2004) and Veselov et al. (2002).
Analysis of root tissues for nutrients
Dry root tissues were finely ground. The concentration of total N was determined using a CHN analyser (Fa. Elementar, Hanau, Germany). Concentrations of P, S, and K were determined using an ICP spectrometer (JY Plus, Division d'Instruments, SA Jobin, Yvon, France).
Statistical treatment of data
The relationship between internal tissue ABA, JV, and JABA was tested for logarithmically transformed data by the Pearson product-moment correlation coefficient after checking for data being normally distributed. The effect of external ABA on the relationship between loge(JV) and loge(JABA) was tested by analysis of covariance (ANCOVA), using loge(JV) as a covariate and ABA treatment as the grouping factor.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Effect of nutrient deficiency on root morphology
Both removal of the caryopses and nutrient deficiency influence root morphology, in particular, weight, diameter, surface area, and branching. When the caryopses had been removed from the maize seedlings before transplanting to hydroponic culture, root weight and surface area of the root were reduced by approximately 32% compared with control plants, whereas the ratio of weight-to-surface area remained constant. In the case of K+ deficiency, this ratio was reduced by about 15%, corresponding with a thinner, more branched root system relative to the full nutrient medium. For root systems grown in CaSO4 or under
deficiency, this ratio increased by about 16% or 29%, respectively, being consistent with a thickened and even less branched root.
Nutrient contents in roots cultivated under conditions of nutrient deficiency
Under N deficiency, N contents of roots was reduced by 58%, P starvation caused a P reduction by 65%, and S deficiency a S reduction by 53%. The reduced K+ content by about 44% under conditions of K+ shortage was compensated by a 7-fold increase of Na and a 42% increase of Ca2+. Although seedlings were germinated in 0.5 mM CaSO4 for 4 d before deficiency treatments, a clear S reduction could be measured (Table 1). Seedlings therefore can be regarded to be deficient of N, P, K, or S, respectively, according to Marschner (2002).
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The role of the caryopsis for radial water (JV) and ABA flow (JABA)
When root systems were taken from seedlings that had been cultivated without their caryopsis in a full nutrient medium, water flow was slightly reduced. Abscisic acid (100 nM) stimulated JV by 55–90% (Table 2). When 5 mM glucose was added to the medium of seedlings without caryopsis, water flows were even higher than those of the controls (Fig. 1a, b; analysis of variance for repeated measurements: F=6.15, df=2,23, P=0.007). The stimulation of JV by ABA for this treatment, however, was only 30% (Table 2). Thus glucose fully replaces the missing carbohydrates of the caryopsis as far as JV is concerned. The stimulating effect of glucose on intact seedlings with the caryopsis was very small and without statistical significance (+4–6%).
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The effect of nutrient deficiency on JV and JABA
The experiments described in this paragraph were performed with seedlings that have been cultivated without caryopses. Glucose was added to the medium as described above. When different nutrients were removed from the nutrient medium, stimulation and inhibition of water flows could be observed. Nitrogen deficiency caused a significant reduction of JV (P=0.008) whereas potassium deficiency stimulated it (P <0.001). Water flows through roots of phosphorus- and sulphur-deficient seedlings, as well as those kept in 0.5 mM CaSO4, remained unaffected. Except in potassium-deficient roots, 100 nM ABA always stimulated the water flow up to 55% compared with control plants without external ABA (Table 2).
A clear stimulating effect (4-fold increase) of nutrient deficiency on ABA flows could only be observed in roots cultivated in 0.5 mM CaSO4 (Table 2; P=0.047). Under potassium deficiency JABA was doubled (Fig. 2a, b; analysis of variance for repeated measurements: F=24.25, df=2,8, P <0.001). Perturbations of the nutrient supply increased the accumulation of endogenous ABA in roots taken from seedlings that had been cultivated under conditions of (P=0.094) and K+ deficiency (3-fold in both cases) (P=0.021).
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Relationship between tissue ABA, JV and JABA
Figure 3a–c shows the relation between tissue ABA and JV and JABA and also the relationship between JV and JABA. Data of all the experiments described above have been used for these plots. The open symbols show the tissue ABA before ABA treatment (endogenous ABA), the closed symbols show the root tissue ABA at the end of the experiment, 120 min after the addition of 100 nM ABA to the medium (also called internal ABA).
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There was a highly significant linear positive correlation (Pearson correlation: N=146, r=0.719, P
0.001) when endogenous and internal ABA was plotted against JABA (Fig. 3a). The differences in the internal ABA of the root hair zone of maize roots allow a prediction about differences in the radial ABA flow to the xylem.
When the endogenous and the internal ABA of maize roots were plotted against the radial water flow (Fig. 3b) a highly significant correlation was again found (N=169, r=0.523, P 0.001). There was also a significant correlation when only endogenous ABA was considered (N=83, r=0.242, P=0.027). The stimulation of JV could be seen within the range of 2–300 pmol g–1 FW.
Relationship between JV and JABA
In Fig. 3c, JV is plotted against JABA. When the flows with and without external ABA addition were analysed separately there was a highly positive correlation between JV and JABA (without external ABA: N=218, r=0.748, P 0.001; in the presence of external 100 nM ABA: N=139, r=0.750, P 0.001), indicating JV and JABA are closely coupled. This tight relationship between JV and JABA, however, was modified by the addition of external ABA (analysis of covariance, N=357, r2=0.664, P <0.001; effect of ABA on JABA: F1,354=110, P <0.001). The dependency of JABA on external ABA is evident from higher values for JABA at a given JV in the case of ABA addition (open symbols) versus endogenous ABA only (filled symbols in Fig. 3a).
The Casparian bands in the endodermis of maize roots under nitrate and potassium deficiency
Oil blue N (=Sudan blue) was used to stain the Casparian bands of the endodermis of maize root cross-sections. In roots grown under deficiency Casparian bands were stained more intensively, whereas under potassium deficiency stainable structures did not show up with Oil blue N.
Immunolocalization of ABA in maize roots
Figure 4 shows fluorescence signals of ABA in root sections that have been obtained from roots in the presence of lateral water transport, caused by a reduced pressure of –0.06 MPa and 100 nM ABA having been added to the medium. In N-deficient roots (Fig. 4b) signals from the exodermis, the cortical cell walls, the radial cell walls of the endodermis, and the metaxylem vessels are clearly stronger than in control roots (Fig. 4a) grown in full nutrient medium. In roots of potassium-deficient seedlings (Fig. 4c), especially the tissues of the stele and the endodermis, exhibit strong ABA signals, indicating an intensive ABA transport into the stele.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Nutrient deficiency caused by the removal of the caryopsis reduces water flows in maize roots whereas ABA flows are stimulated. The radial water transport through roots is reduced when seedlings have been cultivated without their caryopses, even when they have been supplied with a full nutrient medium. Glucose (5 mM) proved to be sufficient even to overcompensate JV. A sufficient carbohydrate supply by the caryopsis seems to be necessary for optimal radial water flows. An explanation for this phenomenon is not possible at present. Removal of the caryopsis also reduces the stimulating effect of ABA on JV. Whereas in an intact system that is fully supplied with nutrients, JV is increased by ABA by approximately 100% (Table 2; see also Hose et al., 2002
; Sauter et al., 2002), stimulation by ABA is only 55% when the caryopsis is lacking, and is even less in the presence of external glucose. It is concluded that an additional unidentified factor, originating from the caryopsis, is necessary to achieve a full stimulation of JV by ABA. A good supply of carbohydrates may be necessary to maintain sufficiently steep pH gradients across the plasma membranes which are needed to allow a sufficient incorporation of undissociated ABA into the plasma membranes. This is necessary for the stimulating effect of ABA on JV and Lpr (Hose et al., 2000; Wan et al., 2004).
To avoid interference of the nutrients in the caryopsis, experiments have been performed with seedlings free of their caryopses and supplied with 5 mM glucose and a nutrient medium that has been modified with respect to the nutrients N, P, K, S, and Ca. Both inhibition and stimulation of water flows through roots from nutrient-deficient plants could be observed. In most cases data from the literature have been confirmed. As previously described by Radin and Matthews (1989), Carvajal et al. (1996), Quintero et al. (1998), Reinbott and Blevins (1999), and Clarkson et al. (2000) nitrogen deficiency reduced water flows, whereas potassium deficiency stimulated it. Different from the literature (Karmoker et al., 1991), Lpr of maize roots appeared not to be sensitive to sulphur although JV was also slightly increased under S deficiency. Water flows through P-deficient roots were also not affected significantly.
Except in K+-deficient root systems, 100 nM ABA, a concentration that resembles the apoplastic ABA concentration in stressed plants, stimulated the radial water flow. Whereas ABA normally doubles the water flow in the intact seedling system, water flow was stimulated by about 30–50%, independent of the specific nutrient that was lacking.
Nutrient deficiency has often been reported to stimulate ABA accumulation in plant tissues. In the experiments reported here only nitrate and potassium deficiency caused substantial accumulations of ABA in the roots. In the case of N deficiency, the observed accumulation may also be a result of a reduced ABA flow across the endodermis. An increased accumulation of ABA in N-deficient roots has often been reported in the past (for references see Peuke et al., 1994). A similar phenomenon has been observed by Peuke et al. (2002) in roots of castor bean plants grown under potassium deficiency. The Casparian bands of the endodermis show stronger incorporation of suberin in roots of N-deficient plants and the visualization of ABA transport by immunolocalization also shows stronger ABA signals in the cortical cells.
In roots taken from seedlings kept under potassium deficiency, both water and ABA flows are increased substantially. In this study, immunolocalization shows particularly strong ABA signals in the stelar tissues of the roots. Water and ABA, because of a weaker suberization of the Casparian bands, may enter the stele more easily, where it is loaded to the xylem vessels and accumulated partially in the stelar symplast.
The data of the experiments of this paper have been used to investigate the relations between the endogenous and internal root tissue ABA and the water and ABA flows. Since data were not normally distributed, they had to be transformed by taking natural logarithms. In view of the wide range of both ABA concentrations and flows of ABA and water, respectively, the resulting linear relationships indicate tight physiological connections between all the parameters which are valid for a broad spectrum of experimental conditions. When endogenous and internal ABA are plotted against JABA, a strong positive correlation over nearly three orders of magnitude of tissue ABA concentration becomes evident. Thus, when tissue ABA concentrations of maize roots are known, predictions can be made about the radial ABA flows under transpiring conditions using the linear relation of Fig. 3a for calibration. These predictions are rather robust since no clear effect of individual treatments (nutrient deficiencies) is evident. A highly significant correlation also exists between the internal ABA concentration in roots and the radial water flow at concentrations above 11 nmol g–1 FW, concentrations which have been achieved when 100 nM ABA was added to the nutrient medium. For both logarithmic relationships the slope of JV with respect to JABA on the internal ABA concentration was significantly below 1. This shows that the increase of water and ABA flows is smaller than the increase of internal ABA concentrations at higher values, and flows may saturate beyond 500–1000 nM ABA g–1 FW. As far as JABA is concerned it may indicate that, in this range, which is clearly above the physiological range of root ABA concentrations, the endodermis may exhibit stronger barrier properties for ABA. In accordance with this conclusion, Freundl et al. (1998) have shown that the reflection coefficient 
of ABA increases with the external ABA concentration.
The data of this study show, for the first time, the relations between internal ABA, water, and ABA flows. Up to now, only the relations to exogenous ABA, often in non-physiologically high concentrations have been described. It is shown here that the endogenous and internal ABA of root tissues exhibits a highly significant positive relation to JV within the range of 2–300 pmol g–1 FW. Such a correlation also can be observed when JV is plotted against JABA on logarithmic scales. With increased lateral water flows ABA flows are also increased. This confirms the findings of Freundl et al. (1998, 2000) that ABA is dragged directly across the Casparian bands with the water flow to the xylem vessels. However, the strong positive correlation can also be shown when only data of plants that have not been treated with external ABA are used for statistical analysis.
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Concluding remarks |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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Under conditions of nutrient deficiencies, as can occur in soils of extreme habitats in combination with water deficiency and salt stress, ABA biosynthesis, radial ABA flow, and radial water flow are closely connected and correlated. This could be demonstrated for a wide range of endogenous and internal ABA concentrations in the relevant root tissues. It shows the extent to which changes of endogenous ABA have to take place to produce the parallel stimulation of Jv and JABA. The co-ordination of these transport processes is of high ecophysiological importance in mildly stressed plants.
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Acknowledgements |
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We are grateful to Professor DT Clarkson for stimulating discussion, to Dr CI Ullrich and Dr Markus Langhans (Technical University Darmstadt) who trained us to use the technique of immunolocalization, to Professor EW Weiler (University Bochum) for the generous supply of ABA-antibodies, to Mr Robin Wacker (University Würzburg) for help with the microtome and the dyeing of suberin, to Miss Bianca Röger for skilful technical help, and to Deutsche Forschungsgemeinschaft (Ha 963-11/1) for financial support.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionConcluding remarksReferences |
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R. Aroca, P. Vernieri, and J. M. Ruiz-Lozano Mycorrhizal and non-mycorrhizal Lactuca sativa plants exhibit contrasting responses to exogenous ABA during drought stress and recovery J. Exp. Bot., May 9, 2008; (2008) ern057v1. [Abstract] [Full Text] [PDF]
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P. C. Beaudette, M. Chlup, J. Yee, and R. J. N. Emery Relationships of root conductivity and aquaporin gene expression in Pisum sativum: diurnal patterns and the response to HgCl2 and ABA J. Exp. Bot., April 1, 2007; 58(6): 1291 - 1300. [Abstract] [Full Text] [PDF]
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