Journal of Experimental Botany, Vol. 52, No. 359, pp. 1269-1276,
June 1, 2001
© 2001 Oxford University Press
Original Papers |
Transport and accumulation rates of abscisic acid and aldehyde oxidase activity in Pisum sativum L. in response to suboptimal growth conditions
Biostress Research Laboratory, J. Blaustein Institute for Desert Research and Department of Life Sciences, Ben-Gurion University of the Negev, Sede-Boqer 84990, Israel
Received 9 August 2000; Accepted 9 January 2001
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Abstract |
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Pea plants (Pisum sativum L.) grown initially in nutrient solutions with adequate nitrogen supply (4 mM NO3-) were transferred to solutions containing salt (50 or 100 mM NaCl), ammonium (4 mM) or a low nitrogen supply (0.4 mM NO3-). No changes of abscisic acid (ABA) content were found in roots of stressed pea plants 9 d after the beginning of the treatments; however, accumulation of ABA in the leaves was observed. Old leaves accumulated ABA to a higher extent than young leaves. Accumulation of ABA in leaves of ammonium-fed plants and plants grown under low nitrogen supply occurred in the absence of both increased ABA xylem loading rate and enhanced aldehyde oxidase (AO, EC 1.2.3.1) activity in roots. Enhanced leaf AO activity was observed in all treatments, with the highest increase in old leaves. Among the three AO isoforms (AO-1, AO-2 and AO-3) detected in extracts of pea leaves, the lowest one AO-3 (highest mobility in the gel) correlated with ABA production and showed the highest increment in response to the treatments. The increase of AO activity detected in leaves after 2 weeks of stress application was less prominent than after 9 d, suggesting a transient enhancement of ABA production following the onset of stress. An increase of ABA xylem loading rate as well as AO root activity 4 d and 9 d after application of the treatments was observed only in salt-treated plants followed by a decrease after 14 d in 100 mM NaCl. Decreased cytokinin (trans-zeatin riboside) delivery rate into the xylem sap was observed in all treatments. The role of abscisic acid and cytokinins as positive and negative growth signals, as well as the involvement of root-generated ABA on ABA accumulation in leaves is discussed.
Key words: Pisum sativum L., ammonium, nitrate, salinity, abscisic acid, aldehyde oxidase, cytokinins, xylem delivery rate.
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Introduction |
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Plant adaptation to stress is mediated by multiple signalling pathways that allow the co-ordination of growth and primary assimilation processes in shoots and roots. Cytokinins (CK) and abscisic acid (ABA) have been considered as signals in root-to-shoot communications (Jackson, 1993
), co-ordinating the supply of water and nutrients by roots to the current growth requirements of the shoot. Leaf growth is more inhibited than root growth when nitrogen availability is limiting, or in drought and salinity. Leaf growth repression under these conditions is in most cases linked to a considerable accumulation of ABA (Chapin et al., 1988; Palmer et al., 1996; Zhang and Davies, 1989; Downton and Loveys, 1981). Abscisic acid is synthesized in roots in response to stress (Parry et al., 1992) and it has been suggested that the root is the source of most or at least part of the ABA accumulated in leaves under salt treatments (Kefu et al., 1991). ABA constitutes a root-to-shoot signal for the regulation of stomatal transpiration under salinity (Bano et al., 1993) or drought (Shashidhar et al., 1996) prior to the development of water deficit in leaves. The increase of abscisic acid transport through the xylem sap was also observed under phosphate deficiency (Jeschke et al., 1997) or when ammonium was present in the medium as the only nitrogen source (Peuke et al., 1994).
Other reports, however, indicated that the leaves of stressed plants are not enriched substantially with root ABA and that the involvement of ABA generated in the root in the regulation of shoot growth is doubtful (Munns and Cramer, 1996). The concentration of ABA in the xylem sap did not rise considerably as a consequence of low nitrogen supply (Goldbach et al., 1975; Peuke et al., 1994; Palmer et al., 1996) or of flooding (Else et al., 1996). These facts suggested that the higher ABA content of leaves could have been caused by higher synthesis in the leaves rather than ABA imported from the roots. It has been pointed out that most of the ABA accumulated in young leaves of water-stressed Ricinus and Xanthium plants and flooded pea plants was the result of synthesis and subsequent transport from wilting old leaves (Zeevaart and Boyer, 1984; Zhang and Zhang, 1994). It has also been proposed that increased ABA in the shoot system of flooded pea plants results from an accumulation of this hormone synthesized in the leaves and that the rate of ABA production was not faster than usual (Jackson and Hall, 1987; Jackson et al., 1988). According to these authors this situation, termed an ‘accumulative’ message of soil environment deterioration (Jackson, 1990), can be expected because leaves of plants with oxygen-deficient roots export less assimilates (Castonguay et al., 1993). Finally, it has been suggested that the highest ABA concentration in the xylem of plants grown under water-deficient conditions arise from synthesis in both the roots (first line of response) and the older leaves (second line of response) (Zhang and Davies, 1989; Bano et al., 1993). Since ABA was found in the phloem sap (reviewed by Hoad, 1995) that can move out of the leaves into the phloem (Zeevart and Boyer, 1984) all these hypotheses seemed to be feasible.
The biosynthetic pathway of ABA is now clear to a large extent (Cutler and Krochko, 1999), but it is not sufficient to establish whether the accumulation of ABA in leaves under stress is a result of in situ synthesis or long-distance transport from roots. ABA biosynthesis in higher plants probably occurs via an indirect pathway involving the oxidative cleavage of xanthophylls, for example, zeaxanthin, violaxanthin and neoxanthin (reviewed by Zeevaart and Creelman, 1988; Walton and Li, 1995). The conversion of abscisic aldehyde (ABAld) to ABA, the last step in the abscisic acid synthesis is considered to be catalysed by aldehyde oxidase (AO, EC 1.2.3.1) (Walker-Simmons et al., 1989). AO is presumably also involved in the biosynthesis of another plant hormone, such as indole-3-acetic acid (IAA), through the oxidation of indole-3-acetaldehyde (IAAld) to IAA (Koshiba et al., 1996). AO belongs to the family of Mo-containing enzymes, which in plants include also xanthine dehydrogenase (EC 1.1.1.204; XDH) and nitrate reductase (EC 1.6.6.1, NR) (Mendel and Schwarz, 1999). MoCo-deficient barley and tobacco mutants lacking AO and XDH activities exhibited a reduced capacity to produce ABA (Walker-Simmons et al., 1989; Leydecker et al., 1995). Plant AO has only been purified from maize coleoptiles (Koshiba et al., 1996), and molecular cloning of a plant AO has been reported for maize (Sekimoto et al., 1997), tomato (Ori et al., 1997; Min et al., 2000) and Arabidopsis thaliana (Sekimoto et al., 1998). It was reported recently that one of the AO isoforms, AO
, found in rosette leaf extracts of Arabidopsis plants, can efficiently oxidize abscisic aldehyde (Seo et al., 2000). When the rosette leaves were detached and exposed to dehydration the expression of mRNA encoding AO increased rapidly. AO and XDH activities in ryegrass increased with salinity and 
although the salinity-enhanced activities were more pronounced in roots than in leaves (Sagi et al., 1998). An increase of AO activity was observed in roots of barley plants in response to ammonium and salinity (Omarov et al., 1998).
In the present work, the role of ABA as a stress signal was studied under different suboptimal growth conditions. It was analysed whether foliar ABA content of stressed pea plants is a result of in situ synthesis or of increased transport from the roots. Changes in the activity of aldehyde oxidase (AO) in different plant organs, with a special emphasis on leaf age, under different stress conditions have been examined. The role of cytokinins as a counterbalance to ABA stress-related signals in root-to-shoot communication are discussed.
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Materials and methods |
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Plant material and experimental conditions
Seeds of Pisum sativum L. (cv. Little Marvel) were germinated in vermiculite moistened with water. After 12 d the seedlings were transferred to aerated nutrient solutions. Plant hypocotyls were wrapped with foam rubber and plants of uniform size were inserted through holes in the lids of 20 l tanks (8 plants per tank) containing half-strength Hoagland nutrient solution (Hoagland and Arnon, 1938
) with adequate nitrogen supply (4 mM 
). These seedlings were allowed to establish for 3–4 d prior to nitrogen and salinity treatments. At this time residual cotyledons were removed from the seedlings. The nitrogen sources used were 4 and 0.4 mM NaNO3 or 2 mM (NH4)2SO4. Salinity consisted of 50 and 100 mM NaCl. The nutrient solutions were renewed once a week and the pH (6.5) of the medium was adjusted daily. Experiments were conducted in a greenhouse with midday temperatures ranging between 25–28 °C and a minimum night temperature of 12–15 °C. Sampling of plants in all treatments was carried out 4, 9 and 14 d after application of the treatments. Plants were separated into roots and young, fully expanded, and old leaves. Fresh samples were used for immediate enzyme assays or frozen in liquid N2 and stored at -80 °C for ABA analysis (see below). Dry weight was determined after drying for 72 h at 65 °C in an oven.
Collection and analysis of xylem sap
The xylem sap of plants in each treatment was collected on harvest days. Plants were removed from the nutrient solution, stems were cut with a sharp blade c. 1.5 cm above the shoot base and the stumps with their entire root systems were fitted into a Scholander-type pressure chamber (Arimad-2, Kibbutz Kfar-Charuv, Israel). A pressure of 0.3 MPa was applied to the root systems and sap was collected with a pipette from the cut surface and immediately transferred to ice-cold Eppendorf tubes. The first drop of flowing sap was discarded. The collected sap was frozen in liquid nitrogen and stored at -80 °C prior to the determination of ABA and cytokinins (see below). Xylem sap of nine plants were pooled together to give three replicates.
ABA and trans-zeatin riboside determination
For abscisic acid measurements, the frozen tissues of pea leaves and roots were ground to a fine powder with liquid nitrogen and suspended in solution consisted of 80% methanol, 2% glacial acetic acid and butylated hydroxytoluene (BHT, 20 mg l-1). The extracts were shaken in the dark for 24 h and then centrifuged in a Centrikon T-124 refrigerated centrifuge at 12 000 rpm and 4 °C for 20 min. Supernatant of tissue extracts or xylem sap was taken up in TRIS-buffered saline, TBS (150 mM NaCl, 25 mM TRIS-HCl, pH 7.5). Hormones were quantified by the Phytodetek-ABA and Phytodetek-t-ZR (trans-zeatin riboside) enzyme immunoassay tests (Sigma, USA) using an ELISA procedure with monoclonal antibodies as described previously (Mertens et al., 1983).
Determination of AO activity
Plant tissues were homogenized immediately after harvesting with acid-washed sand and an ice-cold extraction medium containing 250 mM TRIS-HCl (pH 8.5), 1 mM EDTA, 10 mM reduced glutathione (GSH), and 2 mM dithiothreitol (DTT). A ratio of 1 g tissue to 3 ml buffer (1 : ;3 w/v) was used with leaves and 1 g tissue to 2 ml buffer (1 : 2 w/v) for roots. The homogenized plant material was centrifuged at 27 000 g and 4 °C for 10 min. The resulting supernatant was subjected to native polyacrylamide gel electrophoresis (PAGE) with 7.5% polyacrylamide gel in a Laemmli buffer system (Laemmli, 1970) in the absence of SDS at 4 °C. Each lane in the gel was loaded with 100 µg root proteins or 400 µg leaf proteins. After electrophoresis AO activity staining was developed at room temperature in a mixture containing 0.1 M TRIS-HCl, pH 7.5, 0.1 mM phenazine methosulphate, 1 mM MTT (3[4,5-dimethylthiazol-2-yl]-2,5-diphenyltetrazolium-bromide) and 1 mM substrate (indole-3-aldehyde). Activity of AO was estimated on the basis of MTT reduction, which resulted in the development of specific formazan bands. After activity staining, the gels were scanned to quantify the relative intensity of formazan bands which were directly proportional to enzyme activity (Rothe, 1974) using the NIH Image 1.6 computer software. Native PAGE was carried out with a Protean II xi Cell (Bio-Rad, USA).
Protein determination
Total soluble protein content was estimated by the Bio-Rad Protein Assay, a modification of the Bradford procedure (Bradford, 1976), using crystalline bovine serum albumin as a reference.
Statistics
Results are based on three independent experiments with at least three replicate tissue samples from three to four plants in each treatment. The data were analysed using Duncan's multiple range test.
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Results |
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ABA concentration in tissues
ABA concentrations in the tissues of leaves and roots were determined 9 d after the beginning of the treatments. ABA concentration in root extracts of control plants was 0.8 nmol g-1 DW (4 mM
), and no substantial changes were observed as a result of the stress application (data not shown).
ABA concentrations in the shoots were assayed in young, fully expanded, and old leaves. The young leaves of the plants grown under control conditions (4 mM ) showed the highest content of ABA increasing slightly after application of the treatments (Fig. 1a, b). However, in plants grown under stress conditions the greatest accumulation of ABA was found in old leaves. ABA level in old leaves of plants receiving low nitrogen (0.4 mM ) and salinity of 50 mM NaCl increased by 230% and 300%, respectively. Application of 100 mM NaCl and 4 mM enhanced the ABA content in old leaves by 400%. Also fully expanded leaves exhibited a greater capacity for ABA accumulation under stress conditions. Salinity at a concentration of 100 mM NaCl resulted in a 330% increase of ABA concentration while the rest of the treatments revealed increments of 130% to 200%.
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ABA level in xylem exudates
Concentration and delivery rate of ABA in the xylem sap were measured 4, 9 and 14 d after application of the treatments (Table 1). Only salinity increased ABA concentration in the xylem exudate on days 4 and 9. The level of xylem ABA increased by 180% (day 4) and 90% (day 9) in 50 mM NaCl-treated plants. After 100 mM NaCl application to the nutrient solution the concentration of ABA was higher by 250% (day 4) and 180% (day 9). Calculation of ABA xylem delivery rates showed smaller differences between plants under stress and control conditions: 50 mM NaCl-treated plants exhibited 60% increase and 100 mM NaCl-treated plants showed 100% increase. ABA level in the xylem sap of ammonium-fed plants and in plants grown under low nitrate supply did not show any significant differences on days 4 and 9 of the experiment.
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Fourteen days after addition of 50 mM NaCl to the nutrient solutions, the xylem loading rate of ABA was still maintained higher than in controls (150% of controls) although it decreased by 40% with 100 mM NaCl. A slight increase of ABA xylem delivery rate (
30%) was observed after 2 weeks in plants fed with ammonium or low nitrogen concentration.
Cytokinin level in xylem exudates
Concentration and delivery rate of cytokinin in the xylem sap decreased 9 d after application of all treatments (Table 2 ). Ammonium and low nitrogen application to the medium decreased xylem concentration of trans-zeatin ryboside (ZR) by 60% while salt treatment caused only a 25% drop. Xylem delivery rate of trans-ZR decreased by 30% in 50 mM NaCl-treated plants and around 55% in low nitrogen, ammonium and 100 mM NaCl-treated plants. Similar results were found on the 4th day of the experiment (data not shown).
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Aldehyde oxidase activity
The leaf and root samples were taken 4, 9 and 14 d after application of the treatments. Three bands of AO activity were observed (AO-1, AO-2, AO-3) in leaves with marked differences in mobility during native gel electrophoresis and subsequent staining with indole-3-aldehyde as substrate (Fig. 3a, b). One band of AO activity was detected in root extracts (Fig. 2a, b). AO activity in root increased by 100–200% after 4 and 9 d of salinity application (Fig. 2a; Table 3) which correlated with observed changes in ABA xylem loading rates. Root activity of AO was only 50% higher than in control plants after 14 d of growth in the presence of 50 mM NaCl and, in the case of 100 mM NaCl, it dropped to 40% below the level observed in control plants (Table 3). Ammonium nutrition and nitrogen deficiency did not cause any substantial changes in root AO activity after 4–9 d of treatments, however, on the 14th day a 100% increase of AO activity in both cases was observed.
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Leaf AO activity was determined with three different ages: young, fully expanded and old leaves (Table 4
). The total density of the AO bands under control conditions was highest in old leaves. The old leaves also exhibited the largest increase of AO activity under stress conditions. AO activity in the young leaves did not show any significant changes in all treatments during the experimental period. On the 4th day of the experiment AO activity increased in old and fully expanded leaves of plant grown with ammonium and low nitrogen supply (Table 4). On the 9th day after application of the treatments the total band density of AO activity in old leaves increased 70% in the presence of 50 mM NaCl and low nitrogen treatment, 140% in response to 100 mM NaCl and 200% in ammonium-fed plans. The increase of AO activity detected in leaves after 2 weeks of stress application was less prominent than after 9 d. Among the three AO isoforms (AO-1, AO-2 and AO-3) detected in extracts of pea leaves, the lowest one AO-3 (highest mobility in the gel) correlated with ABA production and showed the highest increment in response to the treatments.
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Discussion |
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The concentration and delivery rate of ABA in the xylem sap increased considerably in pea plants subjected to 50 and 100 mM NaCl after 4 d and 9 d of treatments (Table 1
). The increase of ABA in the xylem exudate correlated with enhanced aldehyde oxidase (AO) activity in roots following salinity application (Fig. 2a; Table 3). AO activity has been shown to increase with salinity and in ryegrass plants although to a more pronounced extent in roots than leaves (Sagi et al., 1998). Enhancement of AO activity was also observed in roots of barley plants grown in the presence of ammonium and salinity. In the same experiment no increase of AO activity was found in barley leaves (Omarov et al., 1998). The roots of salt-stressed pea plants had the capacity to produce ABA but did not accumulate it, maintaining a constant level of the hormone in these organs (data not shown). The activity of root AO in plants receiving 50 mM NaCl decreased to the level observed in control plants after 2 weeks of the experiment (Table 3). At this stage (14 d) the xylem loading rate of ABA in plants with 50 mM NaCl (Table 1) was still maintained higher than in controls, a phenomenon ascribed in some papers to recirculation of ABA produced in the shoot (Wolf et al., 1990). Only about 30% of the ABA transported in the xylem sap of Lupinus albus originated in the root. However, NaCl stress shifted the proportion of ABA synthesis from the shoot to the root, resulting in 55% of the xylem sap ABA that was produced by the root (Wolf et al., 1990). It has been suggested that the increase of ABA xylem concentration resulting from soil drying, arises from synthesis in both roots and the older leaves (Zhang and Davies, 1989). In the opinion of these authors, roots are the primary sensors and signals producers. As soil dries further, a secondary response is switched on by an enhanced signal, i.e. the root initial signal plus a signal produced as a result of the gradual wilting of the older leaves. A similar opinion was supported by Bano et al. (Bano et al., 1993). In pea plants exposed for 4 d to salt stress, enhanced AO activity was observed only in roots (Table 3), AO in leaves was maintained at the level of control plants (Table 4). These data suggest that during the first days of the response to salinity the higher level of ABA found in the xylem sap originated in roots. The increase of ABA synthesis found in roots at the beginning of the salt treatments was followed later by an increase of ABA production in old leaves observed on the 9th day (Table 4). A decrease of ABA xylem delivery rate as well as the AO activity in roots of 100 mM salt-treated plants after 2 weeks of treatment pointed out a temporary period of ABA production following stress application (Table 3).
In pea plants grown with low nitrogen and plants receiving ammonium no increase of ABA xylem loading rate nor enhancement of root AO activity was observed 4 d and 9 d after application of the treatments (Table 1, 3). The slight rise of ABA content in the xylem sap as well as increased AO activity in roots was found after only 2 weeks of the experiment. In plants receiving ammonium or low nitrate supply one may have to consider an alternative stress-induced signal delivered by the root to co-ordinate shoot growth in the early stages of stress response. The alternatives could be the drop in cytokinin (trans-zeatin riboside) supply from the root system that was observed in all treatments 9 d after stress application. Similar results were found on the 4th day of the experiment (data not shown). The drop in cytokinin supply was more pronounced in ammonium and low nitrogen-treated plants than in plants under salt stress (Table 2). The decrease in cytokinin concentration in xylem sap was observed under water stress (Bano et al., 1993; Shashidhar et al., 1996), heat treatment (Itai et al., 1973) and also low nitrogen supply (Wagner and Beck, 1993).
The response of xylem sap ABA to the suboptimal growth conditions applied in the present experiments varied with time and the treatment. A clear role of ABA as a stress signal in root-to-shoot cross interaction is suggested only under salinity conditions, in which an increase of ABA xylem delivery rate was found during the early stages of the stress followed by a decrease later on (Table 1). Under low nitrogen supply and ammonium treatment it is difficult to consider ABA as a root-generated stress signal in organs communication since a slight increase of ABA xylem delivery rate was observed only after 14 d of treatments application.
Accumulation of abscisic acid in leaves of stressed pea plants was observed in all treatments (Fig. 1a, b). Old leaves accumulated ABA to a higher extent than young leaves. The ABA concentration in young pea leaves increased only slightly under stress conditions. Similar observations were reported for sunflower plants exposed to low nitrogen in the medium (Goldbach et al., 1975). However, when plants of Ricinus and Xanthium were water stressed, the youngest leaves accumulated the highest levels of ABA (Zeevaart and Boyer, 1984). The accumulated foliar ABA of salt-treated pea plants may have originated in part in roots in view of the higher ABA xylem loading rate and increased AO activity observed in roots (Table 1, 3). However, leaf ABA accumulation in ammonium-fed plants and plants grown with low nitrate concentration occurred in the absence of a marked increase of ABA xylem loading rate as well as AO root activity. The correlation between the increase of ABA accumulation in leaves and the enhancement of ABA synthesis in situ by changes in aldehyde oxidase activity was examined. Aldehyde oxidase exhibited a broad substrate specificity (Koshiba et al., 1996) and indole-3-aldehyde, the substrate giving the highest AO activity after gel staining, was selected as a substrate to follow the changes in AO activity as affected by stress. Enhanced leaf AO activity was observed in all treatments, attaining the highest levels in old leaves (Table 4) and correlating with the highest levels of ABA accumulation in these organs. Among the three AO isoforms (AO-1, AO-2 and AO-3) detected in extracts of pea leaves, the lowest one AO-3 (highest mobility in the gel) correlated with ABA production and showed the highest increment in response to the treatments as estimated by density measurements (Fig. 3a, b). Also in Ricinus and Xanthium plants the oldest leaves had the greater capacity to produce ABA when detached and dehydrated (Zeevaart and Boyer, 1984). The increase of AO activity detected in leaves after 2 weeks of stress application was less prominent than after 9 d, suggesting a transient enhancement of ABA production following the onset of stress.
Studies reporting organ-specific distribution of aldehyde oxidase activity showed that AO polymorphism of gel electrophoretic bands occurred mainly in leaves of dicotyledons such as pea, tomato (Sagi et al., 1999), and Arabidopsis (Schwartz et al., 1997) and roots of monocots such as barley (Omarov et al., 1999), maize (Barabás et al., 2000) and ryegrass (Sagi et al., 1998). The characteristic band proliferation of AO observed in response to stress seems to take place in roots of monocots and leaves of dicots and may be indicative of the main sites of ABA synthesis. In plants, studies on AO have focused on its possible involvement in the biosynthesis of plant hormones, such as indole-3-acetic acid (IAA) and abscisic acid, although the polymorphism of AO gel electrophoretic bands may be related to the different, specific metabolic roles which have not been established yet.
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Acknowledgments |
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The authors are grateful to Dr Rustem Omarov for critical reading of the manuscript and to Genia Shichman for her excellent technical assistance.
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Notes |
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1 Present address and to whom correspondence should be sent: Biochemistry Department, Warsaw Agricultural University, Rakowiecka 26/30, 02-528 Warsaw, Poland. Fax: +48 22 8499659. E-mail: zdunek{at}delta.sggw.waw.pl
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