JXB Advance Access originally published online on August 13, 2004
Journal of Experimental Botany 2004 55(406):2323-2329; doi:10.1093/jxb/erh240
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RESEARCH PAPER |
Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations
Julius von Sachs Institut für Biowissenschaften der Universität, Lehrstuhl Botanik I, Julius von Sachs Platz 2, D-97082 Würzburg, Germany
* To whom correspondence should be addressed. Fax: + 49 931 888 6158. E-mail: hartung{at}botanik.uni-wuerzburg.de
Received 11 February 2004; Accepted 1 July 2004
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Abstract |
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Using the facultative root hemiparasite Rhinanthus minor and Hordeum vulgare as a host, the flows, depositions, and metabolism of abscisic acid (ABA) within the host, within the parasite, and between host and parasite have been studied. When the plants were supplied with 5 mM
there were weak or no effects of parasitism on ABA flows, biosynthesis, and ABA degradation in barley. However, ABA deposition was significantly affected in the leaf laminae (3-fold) and in the leaf sheath (2.4-fold), but not in roots. Dramatic changes in ABA flows, metabolism, and deposition on a per plant basis, however, have been observed in Rhinanthus. Biosynthesis in the roots was 12-fold higher after attachment, resulting in 14-fold higher ABA flows in the xylem. A large portion of this ABA was metabolized, a small portion was deposited. Phloem flows of ABA were increased 13-fold after attachment. The concentrations of ABA in tissues and transport fluids were higher in attached Rhinanthus by an order of magnitude than in host tissues and xylem sap. The same tendency was also found in a comparison between single Rhinanthus and unparasitized barley. As compared with 5 mM lower 
or 1 mM 
supply doubled the ABA concentrations in barley leaf laminae, while having only small or non-significant effects in the other organs. The possible function of ABA for the parasite is discussed. Key words: Abscisic acid, Hordeum vulgare, long-distance transport, parasitic association, Rhinanthus minor
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Introduction |
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Angiosperm root hemiparasites, such as the facultative one, Rhinanthus minor, or the obligate one, Striga attach to the root system of a host plant and extract xylem sap after gaining contact with xylem vessels. The exploitation of xylem sap is enabled by establishing a continuously high leaf conductance (gs), during the night as well (Taylor and Seel, 1998
; Seel and Press, 1994; Seel et al., 1993; Press et al., 1988; Jiang et al., 2003), whereas the stomata of non-parasitizing Rhinanthus minor plants are almost closed. Water uptake into the root of the parasite is also improved by very high values of hydraulic conductivity (Lpr) of Rhinanthus roots (Jiang et al., 2003). Both, stomatal aperture (gs) and root conductivity in general are regulated by the plant stress hormone abscisic acid (ABA), and high ABA levels have been found in leaves and roots of unattached Rhinanthus minor, which would be consistent with the low gs and high Lpr found in these organs (Jiang et al., 2003). A possible physiological role of ABA in hemiparasitic associations has also been studied by Taylor et al. (1996) and Frost et al. (1997) in the Striga/maize and Striga/Sorghum associations. Taylor et al. (1996) observed ABA to be higher by an order of magnitude in Striga, while it increased 60% in maize leaves after infection by the parasite. The authors suggested that localized water deficiency around the haustoria could stimulate ABA formation in the host roots. Drennan and El Hiweris (1979) and Frost et al. (1997) investigated the Striga/Sorghum association and found increased xylem sap and leaf ABA concentrations in the parasitized host. It was suggested that this extra ABA could be involved in the regulation of the host stomatal conductance, however, clear experimental data are still missing. Lechowski (1996) investigated the ABA relationships in the epidermis of Melampyrum arvense parasitizing on Capsella bursa-pastoris. Before attachment, both Melampyrum and Capsella showed a clear diurnal behaviour of epidermal ABA, with low concentrations during the night. After attachment, the ABA of Melampyrum leaf epidermis remained continuously high, during the night as well. ABA concentration in the xylem sap (ABAxyl) of Melampyrum was increased 5-fold after attachment.
In the experiments in this paper, ABA concentrations in the organs and transport fluids of Rhinanthus minor, Hordeum vulgare, and of the Rhinanthus minor/Hordeum vulgare association have been studied. Using the techniques of Hibberd et al. (1999) and Jiang et al. (2003), ABA flows have been determined in an empirically-based model. The impact of nitrogen nutrition has also been studied, because, as pointed out by Parker and Riches (1993), infection of grassland by Rhinanthus can be controlled more easily by changes in nitrogen fertilization.
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Materials and methods |
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Culture of plants
The cultivation procedures in the experiments, in which the plants were supplied with 5 mM
have been described in detail in Jiang et al. (2003). The plants, parasites, and hosts, supplied with 1 mM and 1 mM were cultivated and studied from March to June. Germination and transplanting occurred as described by Jiang et al. (2003). The plants were watered daily, initially with a quarter-strength nutrient solution containing 5 mM (for the composition of the media, see Jiang et al., 2003). Three days later half-strength solution and, after a further 3 d, full-strength solution was supplied. At 32 d after transplanting (about 21 d after successful attachment), and 9 d before the first harvest, the pots with plants were washed several times with deionized water to remove the nutrient solution containing 5 mM ; then two kinds of nutrient solution containing (in mM): (i) 1 0.4 K+, 1.5 
(ii) 1 
0.4 K+, 1.7 
1.6 Cl– (the concentrations of other elements were the same as described in Jiang et al., 2003) were supplied to the plants. Plants were cultivated in the greenhouse with a photoperiod of 12 h and a light intensity of 180–260 µmol m–2 s–1. Eighty to 100 Hordeum and 400 Rhinanthus seedlings were cultivated in separate pots or together for allowing attachment. Only successfully attached pairs were used for the study. Attached Rhinanthus plants are significantly higher and exhibit the characteristic morphology (bright green, elongated and sharply toothed leaves).
Harvest of plant tissues
In all of the experiments, 41 d and 54 d after planting, corresponding, if applicable, to about 30 d or 43 d after attachment of the parasite to the host, five single unparasitized Hordeum plants, five unattached Rhinanthus plants and five Hordeum/Rhinanthus associations were harvested. Barley plants were separated into leaf laminae, leaf sheaths, and roots, and Rhinanthus plants were separated into leaves, the stem, lateral buds, the inflorescence, and the root. For some analyses and for estimation of flows the shoot tissues were bulked. All plant parts were weighed before and after freeze-drying, and dry tissues were finely ground before analyses.
Collection and analysis of xylem sap and of phloem exudate
In order to collect xylem sap from Hordeum vulgare, tillers were removed shortly after they emerged to allow for successful sealing of the plants in the pressure pots described in detail by Seel and Jeschke (1999). Xylem sap was collected on 11 days during the study period (from 41 d to 54 d after planting) at different times during the days by placing the pots into the pressure pots, sealing off the shoot, and pressuring the pots containing the moistened sand substrate and the root system until xylem sap exudated from incisions of shoot organs (Jeschke and Pate, 1991). Xylem sap was obtained from the main veins of the barley leaves and from the stem base of Rhinanthus plants after shoot excision (Seel and Jeschke, 1999). Phloem exudates were obtained by applying 1.5 ml of 5 mM Na2EDTA to the base of excised barley leaves or Rhinanthus shoots, respectively. EDTA stimulates phloem exudation by chelating Ca2+ and thereby prevents the formation of callose, which would seal sieve tubes after wounding (Wolf et al., 1990). Sap samples were stored at –25 °C prior to analysis. K was analysed using ICP spectrometry. For ABA analysis, see below.
Tetcyclacis treatment
Tetcyclacis (10–5 M), a norbornanodiacetine derivate that inhibits the hydroxylation of the 8' methyl group of ABA and the formation of phaseic acid (PA) (Daeter and Hartung, 1990; Zeevaart et al., 1990) was painted, using a soft brush, on leaves and stems of Rhinanthus in a similar way as described by Jiang et al. (2003). The plants were growing in the botanical garden in Würzburg, parasitizing on different hosts.
ABA analysis
Freeze-dried tissue samples were homogenized and extracted in 80% aqueous methanol solution. Extracts were passed through a Sep Pak C18-cartridge. Methanol was removed under reduced pressure and the aqueous residue was partitioned three times against ethyl acetate at pH 3.0. The ethyl acetate of the combined organic fractions was removed under reduced pressure. The newly obtained residue was taken up in TBS-buffer (TRIS-buffered saline; 150 mmol l–1 NaCl, 1 mmol l–1 MgCl2, and 50 mmol l–1 TRIS at pH 7.8) and subjected to an immunological ABA assay (ELISA) as described earlier (Mertens et al., 1985; Peuke et al., 1994). For quantification of ABA-glucose ester (ABA-GE) the aqueous fraction obtained after partitioning was subjected to alkaline hydrolysis as described by Sauter and Hartung (2000). The ABA released from its conjugate was analysed by ELISA as described above. The accuracy of the ELISA has been verified in earlier investigations (Hartung et al., 1994). Recoveries of ABA during the purification procedures were checked routinely using radioactive ABA and found to be more than 95%. The immunochemicals were generously supplied by Professor Weiler, Ruhr Universität Bochum (Germany).
Modelling of ABA flows
The estimation of ABA flows was based on three assumptions: (i) there are only direct xylem-to-xylem links between barley and the root hemiparasite Rhinanthus (Okonkwo, 1966; Dobbins and Kuijt, 1973); (ii) the transfer of ABA from barley to Rhinanthus is given by the ABA concentration in barley xylem sap and the quantities of water transferred from barley to Rhinanthus. The basis for the calculation of ABA flows were the water flows obtained by Jiang et al. (2003); (iii) in the xylem and phloem mass flow occurs and hence solutes are translocated according to their relative concentrations.
According to these assumptions net xylem flows of ABA (JABA,x), from host root to host shoot, or from host roots to the parasite, are given by the flow of water 
and the concentration of ABA in xylem sap [ABA]x:
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The phloem flow of ABA (JABA,p) was estimated on the basis of the previously obtained flows of K (Jiang et al., 2004) as the product of the ratio of ABA to K+ in phloem exudates [ABA/K+]p and the phloem flow of K+ (JK+,p):
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The differences between the estimated net flows of ABA going into or moving out of an organ and its increment (
ABA) in that organ yielded the net metabolic changes of ABA (JABA,met) either by degradation or by synthesis of ABA:
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If the resulting metabolic changes were negative, then net degradation must have occurred, if they were positive then net synthesis was indicated. The data needed in this calculation are presented in Table 1. They are averages of at least five replications ±standard errors.
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Results |
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Abscisic acid content in single and attached barley and Rhinanthus minor
For unparasitized barley plants supplied with 5 mM
solution, the highest concentrations of ABA have been observed in the leaf laminae, those in leaf sheaths being slightly lower. No significant differences between single and parasitized barley were observed (Fig. 1a, b). Compared with unparasitized barley, the ABA concentrations in single, non-parasitizing Rhinanthus minor were higher by a factor of 5.7 in roots and by 12.7 than in barley leaf laminae (Figs 1a, 2). An obvious increase of ABA was seen in shoots of parasitizing Rhinanthus supplied with 5 mM or 1 mM after attachment to barley (Fig. 2). The only clearly significant effects of N supply can be seen in the ABA concentrations of leaves (Fig. 1a, b): both reduced and replacement of lower by caused 2-fold increases in ABA in unparasitized barley leaf laminae. Small but insignificant differences were seen in leaf sheaths and roots (Fig. 1a, b).
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ABA in the xylem sap and phloem exudate
Xylem sap ABA concentrations of attached Rhinanthus were up to 10.5-fold higher than those of parasitized barley. In barley, the xylem sap ABA was nearly doubled after attachment (Table 2). Compared with 5 mM
low or 1 mM supply slightly increased ABA concentrations in barley and nearly halved them in attached Rhinanthus (Fig. 3a, b). Independently of the different N supply, there was no difference between the ABA concentrations in xylem sap in single and attached Rhinanthus. In Table 2 the ABA/K+-ratios obtained by the EDTA-technique, are also given. They are significantly higher in both single and attached Rhinanthus. They were used for establishing the flow models of Fig. 4.
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ABA flows
For barley, the xylem flows of ABA, on a per plant basis, were somewhat (13%) increased after infection by Rhinanthus (Fig. 4); the estimated ABA synthesis in the root was increased (61%) or slightly increased (17%) in leaf sheaths, while the resulting ABA degradation in leaf laminae was somewhat decreased (–10%). Deposition was significantly increased in the leaf laminae (3-fold) and in leaf sheaths (2.4-fold), but not in roots (Fig. 4).
In response to attachment to the host, dramatic changes in ABA flows on a per plant basis, and in metabolism and deposition, have been observed in Rhinanthus. Biosynthesis in the roots was 12-fold higher after attachment, resulting in a 14-fold higher ABA flow in the xylem. A large portion of this ABA was metabolized in the shoot (nearly 12.5-fold increase in ABA degradation compared with single Rhinanthus), and a fraction of this was deposited (even this fraction was 17.9 times larger than in the unattached controls). Phloem flows of ABA were increased 13-fold after attachment. A significant deposition of ABA also was detected in the haustoria of the Rhinanthus/barley association, which was slightly higher than in the root systems of single and parasitizing Rhinanthus (Fig. 4).
Effect of tetcyclacis
When leaves and stem of parasitizing Rhinanthus were treated with 10–5 M tetcyclacis for 4 d the concentrations of ABA-glucose ester were significantly increased in leaves (77%) and the stem (471%). Free ABA in stems rose by 249% and remained unchanged in leaves (Fig. 5).
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Discussion |
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Abscisic acid concentrations in shoots and roots of single Rhinanthus proved to be higher than in the unparasitized, potential host plant barley by a factor of 15 (Figs 1a, 2). Xylem sap ABA of single Rhinanthus minor was also up to 10 times higher than that of unparasitized barley (Fig. 3a, b). In the Rhinanthus/barley association, leaf ABA of the parasite Rhinanthus was higher by an order of magnitude than in the host, which resembles the situation in the Striga/maize association (Taylor et al., 1996
). In the Striga/Sorghum association, however, Frost et al. (1997) found leaf ABA of the parasite only 1.5-fold and xylem sap ABA 2-fold higher than in the host.
In barley, the ABA concentration was only slightly affected without statistical significance by parasitism (Fig.1a, b). This is different from the Striga/maize system where, at least in the case of one maize cultivar, ABA was 60% increased in leaves, whilst in other cultivars ABA was not affected (Taylor et al., 1996). Compared with plants supplied with 5 mM leaf ABA of single and parasitized barley was stimulated when 1 mM or 1 mM was given. Altered N supplies had no effects on ABA concentrations in shoots and roots of single and attached Rhinanthus. Therefore, it seems to be unlikely that ABA is involved in the possible control of Rhinanthus infection by N-fertilization as suggested by Parker and Riches (1993).
Water deficiency caused a clear additional 2–3-fold increase in the ABA of leaves and stems of attached Rhinanthus (data, not shown).
Data from the present experiments, as shown in Table 1, have been used to calculate ABA flows within the parasite, the host, and within the parasitic association. As Fig. 4 shows, in single barley net ABA biosynthesis was observed in the roots, a large portion of which was indicated to be fed into the xylem whereas only a small part was deposited in the roots. Most of the ABA arriving in the leaf laminae was estimated to be metabolized, approximately 25.6% was retranslocated in the phloem to the roots and the smallest part was deposited. A similar situation was detected in single Rhinanthus, however, with much lower flows and rates of deposition and metabolism. One should not forget that in Rhinanthus these weak dynamics happen upon high levels of tissue-, xylem and phloem sap-ABA concentrations. Parasite attachment had only weak consequences for the ABA flows and deposition in the host. ABA net synthesis in roots is increased by 61%, ABA flows in the xylem and phloem remained more or less unchanged. The clearest effects were observed in the leaf sheaths and leaf laminae where ABA deposition increased 2–3-fold. Dramatic changes, however, happened after attachment in tissues of the parasite Rhinanthus. Net synthesis in roots, xylem flow to the shoot, net metabolism in the shoot and phloem transport on a per plant basis were higher by a factor of 12–14, and ABA deposition in the shoot was increased 18-fold. It is also noteworthy, that ABA deposition in the haustoria was higher than net ABA deposition in the whole Rhinanthus root system. ABA extracted from the host contributed by only 7% to the ABA flowing via the xylem from the Rhinanthus root to the shoot. Nearly 67% of this xylem flow originated from biosynthesis and 26% was recirculated in the root from the phloem to the xylem.
When the plants were supplied with 1 mM or when this nitrate was replaced by 1 mM (as compared with 5 mM ) only the ABA relations of barley were affected. Deposition of ABA in barley leaf sheaths and laminae were increased by lower supply with 1 mM and to a weaker extent also in 1 mM plants. ABA concentrations and flows in parasitizing Rhinanthus, however, were hardly affected by altered N supply. Independently of variations in ABA accumulation of the host plants, in response to altered N-nutrition, the parasitizing Rhinanthus maintained its ABA relations at comparatively unaltered levels.
Most remarkably, roots of Rhinanthus minor plants increased ABA biosynthesis dramatically on a per plant basis after attachment to a host, although they are not exposed to external stress conditions (Fig. 4). Rhinanthus minor, as many other Scrophulariaceae parasites (Hodgson, 1973; Pageau et al., 2000) form large amounts of mannitol as the major assimilate resulting in a high osmotic potential of the cell sap of Rhinanthus tissues. Tissues with high concentrations of an osmoticum such as mannitol may also synthesize and accumulate high concentrations of ABA.
Abscisic acid metabolism is an important mechanism to avoid extremely high ABA concentrations in tissues. In Rhinanthus shoots ABA metabolism was therefore increased 12.5-fold after attachment (Fig. 4). Leaves and stems of parasitizing Rhinanthus, were treated with 10–5 M tetcylacis, a norbornanodiacetine derivative that inhibits hydroxylation of the 8'-C-methyl group of ABA and the formation of phaseic acid (PA). Inhibition of oxidative ABA degradation further doubled ABA in stems, whereas the amount of ABA-glucose ester (ABA-GE) rose 5.7-fold (Fig. 5). In the leaves, the inhibition of PA formation doubled ABA-GE. The ABA concentration remained unaffected (Fig. 5). A diversion of ABA metabolism to conjugation, together with a further accumulation of ABA, was observed earlier by Zeevaart et al. (1990). To avoid an increase significantly above 10–12 000 pmol g–1 DW in the absence of PA formation, conjugation becomes an important mechanism of ABA homeostasis in attached Rhinanthus.
Exudation of ABA from roots also could contribute to avoiding an ABA accumulation. Indeed, using the technique of Neumann and Römheld (1999) ABA exudation rates from Rhinanthus seedling roots (2–3.5 cm) and barley seedlings roots (3.5–4.5 cm) into an ABA-free surrounding medium have been detected (Rhinanthus: 0.033 nmol g–1 h–1; barley: 0.0012 nmol g–1 h–1; authors' unpublished data). ABA exudation has not been included into the flow models of Fig. 4, because it was not possible to check the ABA exudation of the adult root system of attached Rhinanthus. In addition, under natural conditions the soil solution under different plants contains ABA in the low nM range (Hartung et al., 1996) which may significantly reduce exudation (Slovik et al., 1995). Therefore, ABA exudation rates must be lower than those observed in ABA-free medium. Regulation of the Rhinanthus ABA content in the roots by exudation cannot be excluded. However, to include exudation data to the ABA models more experimental data are required.
At present no clear explanations for the function of the extremely high ABA concentrations in attached Rhinanthus can be given. In leaves and roots of single Rhinanthus minor, ABA could keep stomata closed and the hydraulic conductivity of roots high (Jiang et al., 2003). In shoots of attached Rhinanthus, however, where stomata are continuously open, even during the night, a stomatal function of ABA seems to be extremely unlikely.
In the field, attached Rhinanthus wilted severely under conditions of serious water shortage and high air temperatures, whereas host plants which could close their stomata still exhibited high turgor. The wilted Rhinanthus plants, however, recovered completely and rapidly without any symptoms of damage when the external conditions improved slightly (F Jiang, unpublished observation). This lack of damage could be a result of the action of dehydrins or other protective proteins whose formation is regulated under stress by high ABA concentrations. Similar mechanisms have been observed in poikilohydric angiosperms, which also do not show anatomical and morphological adaptions to external stress, and which are, however, protected biochemically by proteins such as dehydrins and others (Hartung et al., 1998).
Putative physiological roles of the high ABA concentrations in haustoria are at present under investigation. It seems to be unlikely that ABA facilitates solute and water tapping. In Rhinanthus haustoria no barriers, whose permeability could be increased by ABA, have to be crossed (Jiang et al., 2004). A regulation of the formation of suberized and lignified cells, as shown earlier by Cottle and Kolatukutty (1982) and Pharis et al. (1981) seems to be more likely.
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Acknowledgements |
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We are grateful to Dr Wendy Seel (University of Aberdeen, UK) for stimulating discussions and helpful advice, to Mrs. Bianca Röger for expert technical help, to Professor EW Weiler (Ruhr-University Bochum, Germany) for the generous supply of immunochemicals, and to Deutsche Forschungsgemeinschaft for generous financial support (SFB 567, TP A6).
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