JXB Advance Access originally published online on November 28, 2003
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Journal of Experimental Botany, Vol. 55, No. 394, pp. 131-136, January 1, 2004
© 2004 Oxford University Press
Plants and the Environment |
Form of Al changes with Al concentration in leaves of buckwheat
Received 30 August 2003; Accepted 3 October 2003
1 Faculty of Agriculture, Kagawa University, Ikenobe 2393, Miki-cho, Kita-gun, Kagawa 761-0795, Japan
2 State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
3 Suntory Institute for Bioorganic Research, Wakayamadai 1-1-1, Shimamoto-cho, Mishima-gun, Osaka 618-8503, Japan
* To whom correspondence should be addressed. Fax: +81 87 891 3137. E-mail: maj{at}ag.kagawa-u.ac.jp
Abbreviation: NMR, nuclear magnetic resonance.
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Abstract |
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Buckwheat (Fagopyrum esculentum Moench. cv. Jianxi) is known as an Al-accumulating plant. The process leading to the accumulation of Al in the leaves was investigated, focusing on the chemical form of Al using 27Al-nuclear magnetic resonance. Leaves with different Al concentrations were prepared by growing buckwheat on a very acidic soil (Andosol) amended with or without CaCO3 (1 or 3 g kg–1 soil). When the Al concentration of the leaves was lower, only one major signal was observed at a chemical shift of 16.1 ppm, which was assigned to an Al-oxalate complex at a 1:3 ratio. However, when the Al concentration of the leaves increased to a high level (e.g. 12 g Al kg–1), an additional signal at a chemical shift of 11.2 ppm was observed. This signal was assigned to an Al-citrate complex at a 1:1 ratio. In the leaf with a high Al concentration, both Al-oxalate (1:3) and Al-citrate (1:1) were detected in marginal and middle parts, while only Al-oxalate was detected in the basal part. The oxalate concentration did not differ very much between leaves with low and high Al concentrations at the same position, while citrate concentration significantly increased with increasing Al concentration when the oxalate/Al ratio became lower than 3.0. As the Al-citrate complex has been demonstrated to be the form of transport in the xylem, the results suggest that when internal oxalate is enough to form a complex with Al at a 3:1 ratio in the leaves with a low Al concentration, Al-citrate converts to Al-oxalate. However, this conversion does not occur in the leaves with a very high Al concentration, resulting in the coexistence of both Al-oxalate and Al-citrate complexes.
Key words: Aluminium form, 27Al-NMR, chelation, Fagopyrum esculentum, organic acid, tolerance mechanism (Al).
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Although Al is toxic to plant growth at micromolar concentrations, some plant species show high resistance to Al (for a review, see Kochian, 1995). Buckwheat (Fagopyrum esculentum Moench.) is a species highly resistant to Al toxicity (Ma et al., 1997b). It has been reported that oxalate is involved in both external and internal detoxification of Al in buckwheat (Ma et al., 1997b). When buckwheat (cv. Jianxi) is exposed to Al, oxalate is rapidly secreted from the root tips (Zheng et al., 1998). The secretion of oxalate is highly specific to Al; neither P deficiency nor other trivalent ions such as La induce the secretion of oxalate. As the secretion is inhibited by anion channel inhibitors such as phenylglyoxal (PG), it is suggested that oxalate is secreted through an anion channel.
On the other hand, buckwheat accumulates Al in the leaves at a high level (Ma et al., 1997b). Experiments with water culture have shown that specific processes for uptake, translocation and accumulation of Al exist in the buckwheat plants, in conjunction with a series of changes in the chemical form of Al (Ma and Hiradate, 2000). The roots take up Al in the form of ionic Al (Al3+) due to a large inwardly directed electrochemical gradient for this ion. Following uptake, Al is chelated with the internal oxalate in the root cells, forming a stable, non-phytotoxic complex of Al-oxalate at a 1:3 ratio. When Al is translocated from the roots to the leaves, Al-oxalate (1:3) is converted to Al-citrate (1:1) in the xylem. When Al-citrate moves from the xylem to the leaf cells, Al-citrate reconverts to Al-oxalate (1:3) (Ma and Hiradate, 2000). Since both Al-oxalate (1:3) and Al-citrate (1:1) are stable Al complexes, the plant must possess special mechanisms for achieving these ligand exchanges, although these remain unknown. The Al-oxalate complex is then sequestered in vacuoles of the leaves (Shen et al., 2002). Therefore, the formation of an Al-oxalate complex (1:3) and sequestering this complex in the vacuoles play an important role in internal detoxification of Al. However, when buckwheat was grown in a very acidic soil (non-allophanic Andosol), its Al concentration was so high that the internal oxalate was not sufficient to form a 1:3 Al-oxalate complex. Thus, the chemical forms of Al were explored in buckwheat leaves with a very high Al concentration. In this paper, it is reported that the forms of Al in buckwheat leaves change with the concentration of Al.
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Materials and methods |
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Plant materials and growth conditions
Eight seeds of buckwheat (Fagopyrum esculentum Moench. cv. Jianxi) were sown directly on to the surface of a non-allophanic Andosol amended with or without CaCO3 at 1 g or 3 g kg–1 soil in a 1.0 l pot. The pH (soil/water=1/2.5 w/w) of this soil was 4.5, and amendment with 1 g and 3 g CaCO3 increased the soil pH to 5.0 and 5.5, respectively. To monitor Al concentration in the soil solution, a non-destructive soil solution sampler was installed in the soil as described by Yanai et al. (1993). On day seven, plants were thinned to four per pot. Plants were grown in a growth cabinet (Tomy, CHF-400, Tokyo, Japan) with a 14/10 h, 25/20 °C, day/night regime, light intensity of 40 W m–2 and 70% RH. The plants were watered with one-fifth strength Hoagland nutrient solution, which contained the following macronutrients (mM): KNO3 (1.0), Ca(NO3)2 (1.0), MgSO4 (0.4), and (NH4)H2PO4 (0.2); and micronutrients (µM): Fe-EDTA (20), H3BO3 (3), MnCl2 (0.5), CuSO4 (0.2), ZnSO4 (0.4), and (NH4)6Mo7O24 (1). The solution was adjusted to pH 4.5, 5.0 and 5.5 with 0.4 M HCl or NaOH, for soil with 0 g CaCO3, 1 g CaCO3 and 3 g CaCO3, respectively. After a growth period of 42–60 d, plants were harvested and separated into cotyledons and individual leaves (first to eighth leaf, numbered from oldest to youngest) for the following measurements.
The soil solution was collected with a syringe every 5 d and its pH was immediately monitored with a compact pH meter (Horiba B212, Kyoto, Japan). The Al concentration was also determined as described below. Each experiment was repeated at least twice with three replicates each.
27Al-NMR measurement
The lower (1st leaf), medium (4th leaf), and upper (7th leaf) leaves of buckwheat (42-d-old) from the 0 g CaCO3 treatment, the 1st and 4th leaves from the 1 g CaCO3 treatment, and the 1st leaf from the 3 g CaCO3 treatment were selected for 27Al-NMR measurements. The 5th leaf of buckwheat (60-d-old) was cut into three parts as shown in Fig. 6 of the Results, i.e. marginal part, middle part and basal part and each part was subjected to 27Al-NMR analyses as described below.
Intact leaves were cut into small pieces and then placed in an NMR tube (5 mm in diameter). The spectra of 27Al-NMR were recorded at 130.32 MHz (DMX-500 spectrometer, Bruker Biospin GmbH, Silberstreifen, Rheinstetten/Karlsruhe, Germany). The acquisition parameters were as follows: the observed frequency range, 62.5 kHz; the number of scans, 512; the data size, 32 k points; the repetition delay time, 1 s per 1 scan. The acquired FID data were Fourier transformed with the exponential broadening factor of 50 Hz to obtain the spectra. AlCl3 (2 mM, pH 4.5) was used as an external reference for calibration of the chemical shift (0 ppm). Standard solution contained 50 mM AlCl3, 75 mM oxalate and 25 mM citrate (pH 4.5).
After NMR analyses, the leaves in the NMR tube were collected and the concentrations of Al, oxalate and citrate in the cell sap were determined by methods described below.
Extraction of cell sap and determination of organic acids and Al
Leaf samples were frozen at –80 °C and then ground to a fine powder by hand. Cell sap was obtained by squeezing the frozen sample with a plastic syringe before it was completely thawed at room temperature. After centrifugation (13 000 g, 10 min), the concentrations of Al and organic acids were determined by the methods described below.
The concentration of oxalate was analysed by HPLC with a Shim-pack IC-A3 (Shimadzu, Kyoto, Japan). The eluant was 10 mM NaH2PO4 and 10 mM H3PO4 (pH 2.5) run at 40 °C at a flow rate of 1.0 ml min–1, and detection at 210 nm. The citrate concentration was determined by HPLC with an ion-exclusion column (SCR-102H, 8 mm x 30 cm, Shimadzu, Kyoto, Japan). The mobile phase was dilute perchloric acid solution (pH 2.1) run at 40 °C, and peaks were detected at 425 nm after reaction with 0.2 mM bromthymol blue, 15 mM NaH2PO4, 2 mM NaOH in 5% methanol (Ma et al., 1997a). The flow rate of both the mobile phase and the reactive phase was 0.8 ml min–1.
For total Al determination, the leaf sample was digested with HNO3 as described previously (Shen and Ma, 2001). Al concentrations in soil solution, leaf, cell sap were then determined by electrothermal atomic absorption spectrometry (Hitachi Z-5000, Tokyo, Japan), after an appropriate dilution with 0.1 N HNO3.
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Results |
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Leaves with different Al concentrations were prepared by growing buckwheat in a very acidic soil (non-allophanic Andosol) with or without CaCO3 amendment at different rates. Application of CaCO3 resulted in a significant decrease in Al concentration of soil solution from 258 µM (0 g CaCO3) to 18 (1 g CaCO3) and to 6 µM (3 g CaCO3) during the growth period. The growth was normal on all soils and did not differ very much except that the plants grown on the soil with 0 g CaCO3 treatment (called 0 g CaCO3 plants hereafter) was slightly smaller. Al concentration in the 1st leaf of 0 g CaCO3 plants reached 12.19 g Al kg–1 DW (Fig. 1), while 1 g CaCO3 and 3 g CaCO3 plants accumulated much less Al, being only about 1/4 and 1/10, respectively, of that in the 0 g CaCO3 plants (Fig. 1). In all plants, the distribution of Al showed a similar pattern, that is, the concentrations of Al in the leaves increased from the youngest leaf to the oldest leaf (Fig. 1). This result is consistent with previous findings obtained with a solution culture (Shen and Ma, 2001), confirming that Al distribution is regulated by both duration and rate of transpiration.
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The chemical form of Al in leaves with different Al concentrations was identified using 27Al-NMR spectroscopy. When leaves with a relatively low Al concentration were subjected to the measurement, only one major signal was observed at a chemical shift of 16.1 ppm regardless of leaf position (Fig. 2). According to the 27Al chemical shift, this signal was assigned to an Al-oxalate complex at a ratio of 1:3 (Ma et al., 1997b). However, an additional signal, at a chemical shift of 11.2 ppm, was observed in the lower (1st) and medium (4th) leaves of 0 g CaCO3 plants (Fig. 3A, B). This signal was assigned to an Al-citrate complex at a ratio of 1:1 based on the chemical shift and other evidence discussed later. By contrast, only one major signal at a chemical shift of 16.1 ppm was observed in the upper (7th) leaf with a lower concentration of Al (Fig. 3C). The intensity of the signal for the Al-oxalate (1:3) complex dramatically increased from the upper leaf to the lower leaves (Fig. 3A, B, C).
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The concentrations of oxalate and citrate in the cell sap of each individual leaf were quantified as well as Al. The oxalate concentration gradually decreased from the old to the young leaves in all plants with different Al concentrations (Fig. 4A). However, there was no big difference in the oxalate concentration of the leaves with the same position among the plants with different Al concentrations. For example, the Al concentration in the cell sap of the 1st leaf of 0 g, 1 g and 3 g CaCO3 plants was 100, 18.6, and 6.43 mM, respectively; however, the corresponding oxalate concentration was 135, 123, and 102 mM, respectively. The concentration of citrate in the leaves was much lower than that of oxalate (Fig. 4B). By contrast with oxalate, citrate concentration did not differ among leaves with different positions in the 1 g and 3 g CaCO3 plants. However, in the 0 g CaCO3 plants, the citrate concentration markedly increased from 19 mM in the 5th leaf to 64 mM in the 1st leaf (Fig. 4B). The molar ratio of oxalate to Al was higher than 3 in all leaves of 1 g and 3 g CaCO3 plants (Fig. 4C), while the ratio was below 3 in the 4th or lower leaves in 0 g CaCO3 plants.
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A previous study demonstrated that the concentration of Al in a leaf was the highest in the marginal part and lowest in the basal part (Shen and Ma, 2001). Therefore, the Al forms in different parts of a leaf were investigated. Leaves of 0 g CaCO3 plants with high Al concentrations were chosen for the identification of Al forms. Two peaks corresponding to Al-oxalate (1:3) and Al-citrate (1:1) were observed in the marginal and middle parts (Fig. 5A, B), while only one major peak corresponding to Al-oxalate (1:3) was observed in the basal part (Fig. 5C). Oxalate concentration in the cell sap did not vary much with the part (Fig. 6), but the citrate concentration in the marginal part was more than double that in the basal part. The oxalate/Al ratio was below 3.0 in the marginal and middle parts, while it was above 3.0 in the basal part.
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Discussion |
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Only a small fraction of plant species accumulates Al at a high level in the above-ground plant tissues (Jansen et al., 2002). Most of them are woody species which have been adapted to acidic soil. Accumulating evidence showed that chelation of Al with small organic compounds plays an important role in the internal detoxification of Al in the Al-accumulating plants although other mechanisms were also proposed (for reviews, see Kochian, 1995; Ma, 2000; Ma et al., 2001; Taylor, 1991). For example, Al was reported to be chelated with catechin in tea leaves (Nagata et al., 1992). In hydrangea, Al is demonstrated to chelate with citrate at a 1:1 ratio in the leaves (Ma et al., 1997a), and with delphinidin 3-glucoside and 3-caffeoylquinic in the sepals (Takeda et al., 1985a, b). In Melastoma, Al was found as complexes with oxalate at 1:1, 1:2 and 1:3 ratios as well as the free ion (Watanabe et al., 1998). Buckwheat is an herbaceous plant which accumulates Al in the top (mainly leaves) (Ma et al., 1997b). It has been demonstrated that Al is present in the form of Al-oxalate at a ratio of 1:3 in the leaves of buckwheat grown hydroponically, where Al concentration in the cell sap is 2 mM (Ma et al., 1997b). However, when the buckwheat was grown in a very acidic soil (non-allophanic Andosol), the Al concentration in the cell sap of the oldest leaf (1st) was as high as 100 mM, while the oxalate concentration was only 135 mM (Fig. 4A). This result indicates that internal oxalate is not sufficient to form a complex with all Al at a ratio of 3:1. In the present study, the Al forms in the leaves with different Al concentrations were therefore identified.
To identify the Al forms in plant tissues, 27Al-NMR spectroscopy was applied. 27Al-NMR spectroscopy provides a non-invasive technique to study the bonding of Al with potential ligands without disturbing the equilibrium of the system (Karlik et al., 1982, 1983). This is extremely important for plant cells with multiple compartmentations because the extraction process may cause artificial recombination between different substances which were originally compartmented. Spectra of 27Al-NMR showed that the chemical forms of Al in the buckwheat leaves change with Al concentration and oxalate/Al ratio. When the Al concentration in the leaf was lower, and the ratio of oxalate to Al was higher than 3, Al was present only in the form of Al-oxalate (1:3), irrespective of leaf position (Figs 2A, B, C, 3C). However, when Al concentration in leaves was higher and the ratio of oxalate to Al was lower than 3.0, an additional signal at a chemical shift of 11.2 ppm was observed in addition to Al-oxalate (1:3) complex (Fig. 3A, B). Even within the same leaf, both the signals at 11.2 ppm and 16.1 ppm (corresponding to Al-oxalate (1:3) complexes) were observed in the marginal and middle parts, where the Al concentration was higher than 1/3 of the oxalate concentration (Fig. 5A, B), while only the Al-oxalate (1:3) complex was observed in the basal part where the Al concentration was lower than 1/3 of the oxalate concentration (Fig. 5C). According to the chemical shift of 27Al-NMR, this signal could be assigned to either Al-oxalate at 1:2 ratio or Al-citrate at 1:1 ratio, which has a chemical shift of 10.8 and 11.2 ppm, respectively (Ma et al., 1997a, 1998; Watanabe and Osaki, 2001). However, together with other evidence, this signal is unlikely to be due to the Al-oxalate (1:2) complex, but mainly to the Al-citrate (1:1) complex. Firstly, although the chemical shifts were similar between Al-oxalate (1:2) and Al-citrate complexes, the line widths are different. The Al-oxalate (1:2) complex is characterized by a sharp spectrum (Ma et al., 1997b), while Al-citrate is characterized by a broad spectrum. The spectra in Fig. 3B and C are identical to that of the Al-citrate complex reported previously (Ma et al., 1997a; Watanabe and Osaki, 2001). Secondly, the intensity of the signal corresponding to Al-oxalate (1:3) was dramatically increased with increasing Al concentration in the leaves (Fig. 3). If the Al-oxalate (1:2) complex forms, this signal for the Al-oxalate (1:3) complex should be decreased. Thirdly, the additional signal at 11.2 ppm was only observed when the oxalate/Al ratio is below 3 (Figs 3, 4). The ratio of oxalate/Al will not be 3 if the complex of Al-oxalate (1:2) forms. Fourthly, the internal citrate concentration was much lower than oxalate and was kept at a constant level in leaves with low Al concentrations (Fig. 4B). However, in the leaves with a higher Al concentration (in 0 g CaCO3 plants) where an additional signal at 11.2 ppm was observed, the concentration of endogenous citrate increased remarkably (Fig. 4B, C). Furthermore, an estimation by GEOCHEM-PC (Parker et al., 1995) showed that the major species was Al-oxalate (1:3) (18.8 mM) and Al-citrate (1:1) (24.9 mM) in a standard solution containing 50 mM Al, 75 mM oxalate, and 25 mM citrate. This estimation is in agreement with the 27Al-NMR spectra (Fig. 2S).
The Al-citrate complex is the form of transport in the xylem (Ma and Hiradate, 2000). The distribution of this Al form in the leaves is controlled by transpiration and, furthermore, Al does not move from one leaf to another (Shen and Ma, 2001). These results, therefore, suggest that at a low Al concentration, when internal oxalate is enough to form a complex with Al at a 3:1 ratio, Al-citrate converts to Al-oxalate in the leaves. However, this conversion does not occur at very high Al concentration, resulting in the accumulation of citrate as a citrate-Al complex in the old leaves and marginal part of a leaf (Figs 3A, B, 5A).
Oxalate was demonstrated to be localized in the vacuole of the buckwheat leaf cell (Shen et al., 2002). Buckwheat leaves contain a high concentration of soluble oxalate, ranging from 32 to 135 mM in the cell sap depending on leaf position. However, in the leaf at the same position, the oxalate concentration did not increase much even when the Al concentration increased several fold (Figs 1, 4A). This result suggests that the biosynthesis of oxalate is not enhanced by increased Al. In a study with solution culture, it was also reported that there is no difference in the concentration of oxalate in the cell sap between buckwheat leaves treated with Al and those without Al treatment (Ma et al., 1998).
The Al-oxalate (1:3) complex is sequestered in the vacuole of buckwheat leaf cells (Shen et al., 2002), however, the localization of Al-citrate is unknown. An attempt was made to localize this complex by isolating protoplasts and vacuoles, but it was not successful. This might have been due to the age of the leaves, because only old leaves contain both citrate-Al and oxalate-Al.
Both the Al-citrate and Al-oxalate (1:3) complexes are non-phytotoxic forms of Al (Ma et al., 1997a, b, 1998). Therefore, even in a leaf that accumulated high Al (12 g kg–1), no toxicity symptoms were observed. However, in the leaves with a very high concentration of Al, the leaf size was slightly smaller compared with those with less Al accumulation. The exact reason for this phenomenon is unknown. One possible explanation is that high accumulation of citrate as the citrate-Al complex may affect the growth. Citrate is an important intermediate in many metabolic processes. When Al concentration is low and internal oxalate is sufficient, the free-citrate released during the process of conversion from Al-citrate to Al-oxalate (1:3) may be reused for the conversion or incorporated in the metabolism. However, high accumulation of citrate as an Al-citrate complex limits the utilization of citrate. Since Al accumulation increases with increasing Al concentration in the soil solution (Fig. 1), buckwheat seems to lack feedback control of Al uptake. From this point of view, the accumulation of Al in the form of Al-citrate is also an important mechanism for the internal detoxification of high Al in buckwheat.
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Acknowledgements |
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This research was supported in part by a Grant-in-Aid from the Ministry of Education, Science, Sports, and Culture of Japan (Grant no. 15208008 to JF Ma) and by ‘Outstanding Talent Recruitment from Overseas’ programme of the Chinese Academy of Sciences (to R Shen). Renfang Shen was the recipient of a Postdoctoral Fellowship from the Japan Society for the Promotion of Science.
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