Journal of Experimental Botany, Vol. 51, No. 346, pp. 929-935,
May 2000
© 2000 Oxford University Press
Radial transport of abscisic acid conjugates in maize roots: its implication for long distance stress signals
Julius von Sachs Institut für Biowissenschaften der Universität Würzburg, Lehrstuhl Botanik I, Julius von Sachs Platz 2, D-97082 Würzburg, Germany
Received 18 October 1999; Accepted 7 January 2000
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Abstract |
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Conjugated, alkaline hydrolysable ABA (predominantly abscisic acid glucose ester, ABA-GE), which is transported in the xylem from roots to shoots of Zea mays L. plants, has its origin in the root symplast rather than from soil, although it was detectable in soil solution with concentrations up to 30 nM. External ABA glucose ester cannot be dragged with the water flow across the exodermis and the endodermis because of its hydrophobic properties. Experimental evidence is presented that enzymes in the cortical apoplast cleave ABA-GE thus releasing ABA from its conjugates. Liberated ABA can then be translocated apoplastically and symplastically to the xylem vessels. Endogenous ABA-GE can be released from isolated cortical and stelar tissues to the surrounding media, with rates that are up to 5-fold higher from stelar tissues than those from cortical tissues. Release of ABA-GE is highest under conditions of inhibited ABA-metabolism.
Key words: ABA and ABA glucose ester, Zea mays L., roots, xylem sap, soil.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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It has been discussed recently that ABA conjugates may act as root to shoot stress signals. Several authors (Bano et al., 1993
, Bano, 1994; Hansen and Dörffling, 1999; Hartung et al., 1999; Hartung and Jeschke, 1999; Jeschke et al., 1997a, Jeschke1et al1997b) have detected glucose esters of abscisic acid (ABA-GE) and phaseic acid in the xylem sap of drought and salt-stressed plants of Oryza sativa, Helianthus annuus, Zea mays, Ricinus communis, and Anastatica hiërochuntica.
However, it is unknown how ABA-GE is transported within the roots and released from the root symplast to the xylem vessels. The question arises whether ABA conjugates are taken up by mesophyll cells after arrival in the leaf apoplast since the permeability coefficient of plasma membranes for ABA-GE is extremely low (10-11 ms-1, Baier et al., 1988). Additionally, it has to be taken into account that ABA-GE is physiologically inactive (Walton, 1983) and needs to be hydrolysed before it can act on guard cells and meristems. The fate of ABA-GE in the leaf apoplast of barley has also been investigated (Dietz et al., 2000). An ABA-GE-cleaving, apoplastic ß-D-glucosidase which releases ABA from its conjugate has been detected.
This paper deals with the radial transport and release of ABA-GE to the xylem vessels in Zea mays L. roots with a view to establishing possible roles for apoplastic barriers (exodermis and endodermis). Investigations have been done concerning the origin of xylem sap ABA-GE (e.g. external soil solution or cortex symplast). Furthermore, the existence of an ABA-GE cleaving enzyme in the intercellular washing fluid (IWF) of maize roots could be detected.
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Materials and methods |
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Collection of soil samples
Soil samples to a depth of 50 cm were obtained using an auger. The samples were taken from agricultural fields near Würzburg beneath a range of crops including maize (Zea mays L.), wheat (Triticum aestivum L.), rye (Secale cereale L.), sunflower (Helianthus annuus L.), and potato (Solanum tuberosum L.).
Soil moisture is expressed as the percentage of the water-holding capacity (WHC). It was measured gravimetrically by weighing fresh soil, dried soil (24 h at 105 °C) and water-saturated soil.
Preparation of soil samples for ABA and ABA-GE analysis
Fresh soil samples (4 g) were extracted with 8 ml of 10 mM CaCl2 for 24 h at 4 °C. The aqueous soil extracts were acidified with 0.1 M HCl to pH 3.0 and partitioned three times against ethyl acetate. The organic fractions were collected and reduced to dryness, taken up in TBS-buffer (TRIS-HCl: 50 mM TRIS, 150 mM NaCl, 1 mM MgCl2, pH 7.8) and subjected to ABA assay by ELISA as described earlier (Weiler, 1986). The aqueous fractions which contain ABA-conjugates were hydrolysed with NaOH (1 M) for 1 h, adjusted to pH 3.0 with HCl and partitioned against ethyl acetate as described above. ABA, released from ABA conjugates was determined by ELISA.
Plant material for radial transport of ABA-GE
Seeds of maize (Zea mays L. cv. Garant FAO 240; Asgrow, Bruchsal, Germany) were germinated on filter paper soaked with 0.5 mM CaSO4 for 4–5 d at 25 °C in the dark. The seedlings developed primary roots of up to 10 cm and coleoptiles of up to 3 cm in length. Some of the seedlings were transferred to aerated hydroponic culture pots (100 ml). The nutrient solution consisted of 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 a pH of 5.5. The plants were 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). To obtain roots with an exodermis, seedlings were grown in a mist culture (aeroponics) using the same nutrient solution. Seedlings were fixed by pieces of foam rubber in holes on the top of a PVC box of 1 m3 (Zimmermann and Steudle, 1998) whereby the roots protruded into the box. A clock-regulated air conditioner (‘Defensor’ from Axair GmbH; Nürnberg, Germany) producing mist for a total of 10 h d-1 was placed at the bottom of the box. The growing conditions of the aeroponic culture were similar to those used for hydroponic culture (see also Freundl et al., 2000). Plants were cultivated for 8 d either in hydroponics or in aeroponics. A description of the root and shoot anatomy for both cultures has already been published (Zimmermann and Steudle, 1998).
Root surface area
Root surface areas were determined by using an image analysing system based on a video camera and software (DIAS from Delta-T Devices; Cambridge, UK). The measurements were performed as described previously (Freundl et al., 1998). Surface areas from roots grown in hydroponic and in aeroponic cultures were between 0.0046 and 0.0092 m2 and between 0.0047 and 0.0124 m2, respectively.
Collection of xylem sap
Seedlings grown under aeroponic conditions were transferred to pots containing aerated nutrient solution (see above). Hydroponically and aeroponically cultivated seedlings were decapitated directly above the mesocotyl. The excised root system including the mesocotyl was attached to a capillary by a pressure-tight silicone seal. The capillary was connected to a vacuum pump and the suction pressure could be regulated with a manometer. A detailed description of the experimental set-up has been published (Freundl et al., 1998). A sub-atmospheric pressure of -0.045 MPa was applied to the xylem of the excised root systems which caused a xylem flow into the capillary. It should be mentioned that sub-atmospheric pressure was used as the reference (zero pressure) throughout this paper. After 20 min the flow of water across the root system was steady and the xylem sap was collected with a syringe at 20 min intervals. Abscisic acid glucose ester (100 nM; purchased from Apex Organics, Honiton, UK) was added to the nutrient solution after 80 min. Water flow was determined by weighing harvested xylem sap fractions.
When the effect of salt stress was investigated, seedlings were cultivated for 4 d in a medium containing 50 mM NaCl and another 4 d with enhanced salt concentration of 100 mM. To obtain sufficient amounts of xylem sap for ABA and ABA-GE analysis the root systems had to be kept in a NaCl-free medium during the application of sub-atmospheric pressure.
A separate experiment showed a 50% inhibition of root and shoot growth within a cultivation period of 3 weeks when 100 mM NaCl was added to the culture medium (not shown).
Analysis of free and conjugated ABA
Xylem sap samples were taken up in TBS-buffer and analysed for free and conjugated ABA as described above.
Experiments with root cortical and stelar segments
Segments of 7-d-old maize seedlings, 3 cm in length, were cut 1.5 cm behind the root tip and divided into root cortex and stele. The separation of the tissues occurred at the endodermis. Six segments were washed three times for 10 min in 3 ml of a buffered nutrient solution (0.2% (w/v) bovine serum albumin (BSA), 2 mM CaCl2, 3 mM KCl, 1 mM K2HPO4, 0.01 mM tetcyclacis, 0.2% (w/v) polyvinyl-pyrrolidone (PVP) 40, 25 mM MES-KOH at a pH of 6.0, 2 mM ascorbic acid, and 2 mM cysteine) and transferred to 3 ml incubation medium (2 mM CaCl2, 1 mM glucose, 6 mM KCl, 2 mM K2HPO4, 1.5 mM KNO3, 1 mM MgSO4, 100 U ml-1 penicillin, 25 mM MES-KOH (pH 6.0), and 10-5 M tetcyclacis, 100 mM NaCl, and 5 or 50 nM ABA (Sigma, Deisenhofen, Germany)) for 24 h. Tetcyclacis is a norbornanodiacetine derivative that prevents oxidative degradation of ABA to phaseic acid (Zeevaart et al., 1988; Daeter and Hartung, 1990). The incubation medium was replaced by an ABA-free medium and after certain time intervals (Fig. 4) the media were analysed for free and conjugated ABA. The validity of the ELISA for Zea mays L. has been confirmed earlier (Hartung et al., 1994).
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Intercellular washing fluid (IWF) of root segments
Eleven-day-old hydroponically cultivated maize seedlings were used. The whole root system was infiltrated with a solution containing 0.5 mM CaCl2 at about -10 Pa for 15 min. The surface of the infiltrated root system was dried with a tissue after release of the vacuum. The roots were placed into tubes with perforated bottoms (2.2 cm diameter) which were inserted in centrifugation tubes 2.7 cm diameter. The segments were centrifuged at 2000 g for 20 min. IWF was collected and used immediately for experiments or stored at -80 °C until further use.
Determination of ß-D-glucosidase activity
The standard enzyme assay contained 400 µl of 100 mM citrate buffer adjusted to pH 4.8 with KOH. p-Nitrophenol-ß-D-glucopyranoside (pNPG) was used as a substrate and dissolved in dimethylformamide (200 mg ml-1). Ten µl of the substrate stock solution and 10 µl IWF were added to the buffer. After 60 min of incubation at 37 °C, the reaction was stopped by adding 1 ml of 200 mM Na2CO3 solution. The amount of liberated p-nitrophenol was quantified spectrometrically at 405 nm using the molar extinction coefficient 
=18.300 
Abs * l * (mol cm)-1 (Del Campillo and Shannon, 1982).
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Results |
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ABA conjugates in soil solutions
Aqueous extracts of soil samples from agricultural fields near Würzburg have been analysed for ABA-glucose ester (ABA-GE). Assuming that all ABA-GE is dissolved in the soil water at the time of sampling ABA-GE concentrations ranged from 0.4 (under sunflower in calcareous soil) to 35 nM (under sunflower in sandy soils). In accordance with earlier work (Hartung et al., 1996
) no consistent changes of free ABA concentration with soil depth were detected (data not shown). However, the ABA-GE concentration decreased with depth in five out of the six fields (Table 1).
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As the soil dried, the concentration of ABA-GE increased in the soil solution (Fig. 1
). Compared to free ABA the concentration of ABA-GE rose by a factor of 6. The dashed lines illustrate the theoretical effect of water removal, by crop and soil evaporation, on the ABA-GE concentration.
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Radial transport of ABA-GE
Sub-atmospheric pressure of -0.045 MPa has been applied to the cut surface of the mesocotyl of maize seedlings to induce a water flow from the surrounding medium to the xylem vessels (Freundl et al., 1998). Endogenous abscisic acid from xylem sap samples of hydroponically cultivated maize seedlings ranged between 0.2 and 0.4 nM (Fig. 2A). Although ABA-GE was added to the external nutrient medium, the concentration of the conjugate decreased in the xylem within the following 60 min. The concentration of free ABA, however, increased simultaneously from 1.1 nM up to 8.0 nM in the xylem. As ABA concentration rose, the radial water flow (JVr) of the root system also increased by a factor of 1.5 (Fig. 2C).
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The same type of experiment has also been performed with aeroponically cultivated roots which have an exodermis. Casparian bands developed under the whole root hair zone down to 3 cm above the root tip (Freundl et al., 2000
). The concentration of endogenous ABA (2.2–4.6 nM) in the xylem sap was higher, on average, by a factor of 11 compared to roots devoid of an exodermis. When ABA-GE was added to the medium no significant increase of free ABA (2.3–5.2 nM) could be observed. ABA-GE concentration ranged between 1.1–2.6 nM. After 120 min it decreased slightly, but remained detectable throughout the experiment. The radial water flow (JVr) was virtually unaffected under these conditions (Fig. 2D
).
ß-Glucosidase activity in the intercellular washing fluid of maize root segments
The intercellular washing fluid (IWF) of excised maize root systems was assayed for ß-glucosidase activity using p-nitrophenol-ß-D-glucopyranoside as the substrate. When increasing ABA-GE concentrations were added to the assay (Fig. 3), the enzyme activity was reduced by 48%, suggesting that ABA conjugates can serve as a substrate for ß-glucosidases of the root apoplast.
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Release of ABA-GE from root cortical and stelar segments
Three cm long root segments of 7-d-old maize seedlings were separated into root cortex and stele and incubated for 24 h with 5 nM ABA (Fig. 4A), 50 nM ABA (Fig. 4B), and 50 nM ABA plus tetcyclacis (Fig. 4C) and 50 nM ABA plus tetcylacis plus 100 mM NaCl (Fig. 4D). The segments were transferred to a hormone-free nutrient solution and the release of ABA-GE to the medium measured by ELISA. Under all conditions stelar tissues released more ABA-GE to the medium than cortical tissues (Fig. 4A, B, C, D). This was conspicuously the case when segments were preloaded with 10-5 M tetcyclacis which inhibits ABA degradation and increases ABA-GE formation (Zeevaart et al., 1988). Salinity (100 mM NaCl) as an environmental stress factor inhibited the release of ABA-GE from stelar segments. A similar low releasing rate from stelar tissues could be observed when preloading occurred with only 5 nM ABA.
To study the release of ABA-GE and free ABA from the xylem parenchyma cells to the xylem vessels in a more intact system, xylem sap was obtained in a suction experiment as described above and analysed by ELISA. Xylem sap of control root systems contained 0.24±0.05 pmol ABA-GE g-1 FW h-1, whereas in plants pre-treated with 100 mM NaCl this rate was increased up to 0.69±0.17. The release of free ABA was stimulated by salt pre-treatment up to 11-fold (pmol g-1 FW h-1).
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Discussion |
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It has been shown repeatedly in the past that conjugated abscisic acid can be translocated in the xylem sap from roots to shoots of stressed plants. Conjugated ABA was detected in drought-stressed rice and sunflower plants (Bano et al., 1993
, Bano, 1994), in castor beans (Jeschke et al., 1997a; Hartung et al., 1999) and in heavily salt-stressed Anastatica hiërochuntica (Hartung and Jeschke, 1999). Five ABA conjugates have been found in the xylem sap of well-watered sunflower plants (Hansen and Dörffling, 1999). Under drought stress their concentration rose substantially and a sixth conjugate appeared in significant amounts. One of those conjugates was identified as ABA-glucose ester.
The ABA glucose ester could originate from external and internal sources. The soil solution under different crops contained ABA-GE in concentrations up to 30 nM. Different from free ABA (Hartung et al., 1996), the concentration of the conjugate tended to be diluted with soil depth due to the rising water content of the soil.
The data of Fig. 2A make it seem rather unlikely that conjugated ABA is translocated in significant amounts from the soil solution to the xylem of hydroponically cultivated plants even though these roots lack a complete exodermis. Although 100 nM ABA-GE had been added to the nutrient solution, its concentration in the xylem decreased. Simultaneously, an increase of free ABA in the xylem sap was detected, suggesting cleavage of ABA-GE by an apoplastic enzyme. ABA thus liberated can be redistributed to the cortical symplast or dragged with the water flow across the endodermis, as has been shown recently (Freundl et al., 1998). Additionally, water flow (calculated from the data of Fig. 2C) rose from 5.7x10-9 m2 s-1 to 8.4x10-9 m2 s-1. As is known from literature, ABA alters the hydraulic conductance of roots and, therefore, water flow across them. Although this topic has promoted much controversy, it has been claimed that ABA decreased the hydraulic conductivity of roots (Markhart et al., 1979; Fiscus, 1981). It has also been pointed out that ABA stimulates the water flow through plant roots while a gradient in hydrostatic pressure was imposed comparable to that of a transpiring plant (Glinka, 1977, Glinka, 1980; Freundl et al., 1998, 2000). This being the case, the observed decrease of ABA-GE in the xylem could be explained by dilution.
The increase of free ABA in the xylem may be due to an esterase activity in the cortex apoplast. Indeed, intracellular washing fluid of maize roots contained a ß-glucosidase activity which could be inhibited by ABA-GE (Fig. 3). The inhibition reached almost 50%, implying that ABA-GE can serve as a substrate of extracellular ß-glucosidases in maize cortical tissues.
When sub-atmospheric pressure was applied to aeroponically cultivated excised root systems no increase of free ABA in the xylem after adding ABA-GE to the external medium could be observed (Fig. 2B) and water flow remained unaffected. It is concluded that the exodermal layer which is formed in maize roots grown aeroponically (Peterson, 1988; Steudle and Peterson, 1998) acts as an effective barrier for ABA-GE. Thus, the conjugates would not have been taken up into the cortical apoplast and would not have been cleaved by apoplastic glucosidases. Since the water flow remained constant after external ABA-GE addition, dilution of ABA-GE in the xylem could have taken place, assuming that stelar tissues released ABA-GE at constant rate.
Endogenous ABA-GE, which is formed in the root symplast, must be released to the xylem from the stelar parenchyma cells. The experiments shown in Fig. 4 demonstrated that ABA-GE can be released from root cells, however, with particularly high rates from stelar tissues. The highest release was observed under conditions that stimulated ABA-GE formation, such as treatment with tetcyclacis. Surprisingly, treatment with 100 mM NaCl significantly reduced the release of ABA-GE to the medium. In an intact system, however, salt stress (100 mM NaCl) increased the efflux of ABA-GE into the xylem 3-fold.
It has been pointed out (Baier et al., 1988) that the permeability coefficient of ABA-GE for plant plasma membranes is very low. Therefore, a substantial diffusion of ABA-GE to the medium seems to be extremely improbable. Transport of different conjugates across biomembranes may be mediated by ABC-transporters since a great number of ABC transporters are already known with an enormous specificity for a given substrate (Higgins, 1992). Recently, evidence was provided (Sidler et al., 1998) that an AtPGP1 transporter is localized in the plasmalemma of Arabidopsis thaliana seedlings in both root and shoot and this is likely to be involved in hormone-regulated developmental processes.
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Acknowledgments |
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We are grateful to Deutsche Forschungsgemeinschaft (SFB 251, TPA 3) for financial support and to Professor EW Weiler (Lehrstuhl für Pflanzenphysiologie, Universität Bochum, Germany) and Dr W Rademacher (BASF, Limburgerhof, Germany) for the generous supply of immunochemicals and tetcyclacis. We thank Professor K-J Dietz (Lehrstuhl für Stoffwechselphysiologie und Biochemie der Pflanzen, Universität Bielefeld, Germany), Professor DT Clarkson (Long Ashton, UK) and E Hose (Lehrstuhl Botanik I, Universität Würzburg, Germany) for stimulating discussions. The expert technical assistance of B Dierich (Lehrstuhl für Botanik I, Universität Würzburg, Germany) is gratefully acknowledged.
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Notes |
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1 To whom correspondence should be addressed. Fax: +49 931 888 6158. E-mail:hartung{at}botanik.uni-wuerzburg.de
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Abbreviations |
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ABA, abscisic acid; ABA-GE, abscisic acid glucose ester;
, ABA concentration in the xylem; 
, ABA-GE concentration in the xylem; JVr, volume flow per unit root surface area.. |
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