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. 2004 Nov 16;95(2):379–385. doi: 10.1093/aob/mci032

Interactive Effects of Al, Ca and Other Cations on Root Elongation of Rice Cultivars Under Low pH

TOSHIHIRO WATANABE 1,*, KENSUKE OKADA 2
PMCID: PMC4246835  PMID: 15546924

Abstract

• Background and Aims As with other crop species, Al tolerance in rice (Oryza sativa) is widely different among cultivars, and the mechanism for tolerance is unknown. The Ca2+-displacement hypothesis, that is, Al displaces Ca2+ from critical sites in the root apoplast, was predicted to be the essential mechanism for causing Al toxicity in rice cultivars. If displacement of Ca is an essential cause of Al toxicity in rice, Al toxicity may show the same trend as toxicities of elements such as Sr and Ba that are effective in displacing Ca.

• Methods The interactive effects of Al, Ca, Sr and Ba on root elongation of rice cultivars with different Al tolerances were evaluated in hydroponic culture. Al and Ca accumulation in root tips was also investigated.

• Key Results and Conclusions Not only Al but also Sr and Ba applications inhibited root growth of rice cultivars under low Ca conditions. As expected, rice cultivars more tolerant of Sr and Ba were also tolerant of Al (japonica > indica). Although Mg application did not affect Sr or Ba toxicity, Mg alleviated Al toxicity to the same level as Ca application. In addition, Ca application decreased the Al content in root tips without displacement. These results suggest that Ca does not have a specific, irreplaceable role in Al toxicity, unlike Sr and Ba toxicities. Alleviation of Al toxicity with increasing concentrations of Ca in rice cultivars is due to increased ionic strength, not due to decreased Al activity. The difference in Al tolerance between indica and japonica cultivars disappears under high ionic strength conditions, suggesting that different electrochemical characteristics of root-tip cells are related to the significant difference in Al tolerance under low ionic strength conditions.

Keywords: Aluminium tolerance, aluminium toxicity, barium toxicity, Ca2+-displacement hypothesis, Oryza sativa L., root cell walls, strontium toxicity, Triticum aestivum L

INTRODUCTION

Although the primary mechanism of Al toxicity remains unclear, the Ca2+-displacement hypothesis has been discussed for a long time. This hypothesis proposes that Al displaces Ca2+ from critical sites in the apoplast and is supported by many reports in which Ca application alleviates Al toxicity symptoms in plants (Hecht-Buchholz and Schuster, 1987; Noble et al, 1988a, b; Shen et al., 1993). Noble et al. (1988a, b) reported that soybean root growth showed a high correlation with an index, CAB (Calcium–Aluminium Balance) that was calculated by [Al3+], [Al(OH)2+], [Al(OH)2+] and [Ca2+] in the medium. Based on these results, displacement of Ca by Al from critical sites in roots has been suggested as an essential cause of Al toxicity. Blamey (2001) proposed three ways that Al accumulated in root cell walls could have a toxic effect: (1) a decrease in apoplastic sorption of basic cations, especially Ca, could reduce nutrient acquisition per unit root length; (2) Al absorbed in the cell wall reduces cell expansion, thereby reducing root elongation; and (3) a reduction in nutrient uptake through decreased root proliferation through the soil.

In contrast, Kinraide et al. (1994) reported that the alleviation of Al toxicity in wheat was not the specific effect of Ca, but was caused by a decrease in Al toxicity on the membrane surface resulting from a decrease in membrane-surface negativity by increased activity of cations (including Ca). In addition, it was reported that in wheat Al did not inhibit Ca uptake even when root elongation was inhibited (Ryan et al., 1994). Furthermore, Al toxicity was alleviated by high concentrations of Mg2+, Sr2+, or Na+ in the medium, although these cations decreased Ca2+ accumulation by the roots (Ryan et al., 1997). These reports indicate that Ca2+-displacement in roots is not an essential cause of Al toxicity in these species.

Rice is known as an Al-tolerant crop (Ishikawa et al., 2000), although its tolerance is widely different among cultivars (Tang Van Hai et al., 1989; Jan and Pettersson, 1993), and the mechanism of Al tolerance in rice is still unclear. Organic acid secretion from roots is considered as one of the most important mechanisms of Al tolerance for some crops, for example in wheat (Delhaize et al., 1993), maize (Pellet et al., 1995) and soybean (Yang et al., 2000). However, organic acid secretion from roots is not a primary mechanism for tolerance in rice (Ishikawa et al., 2000). Recently, Okada et al. (2003) reported that the relative yield of Al-sensitive varieties of upland rice was correlated with the exchangeable Ca in highly weathered soils with low cation exchange capacity (CEC) (Oxisols), suggesting that Ca has an important role in acidic soil Al tolerance of rice.

Sr and Ba, non-essential elements in the same group of elements as Ca, are expected to inhibit root growth by displacement of Ca. Although little is known about the effect of these elements on plant growth, very high concentrations of Ba show toxicity in plants (Chaudhry et al., 1977; Davis et al., 1978). If displacement of Ca from critical sites in roots is an essential cause of Al toxicity in rice, Al toxicity may show the same trend as toxicities of other elements within the same group as Ca. Therefore, in this paper, we examined the interactive effects of Al, Ca, Mg (an essential element from the same group as Ca), Sr and Ba (non-essential elements in the same group as Ca), and Na (a non-essential, alkaline metal) on root elongation of rice cultivars with different Al tolerances, and verified whether the Ca2+-displacement hypothesis could be demonstrated as a mechanism for Al toxicity of rice cultivars. Moreover, since the site of Al toxicity is localized to the root apex (Kochian et al., 2004), Al and Ca contents and root CEC in root apices were determined.

MATERIALS AND METHODS

Germination

The seeds of rice cultivars were surface-sterilized with sodium hypochlorite for 10 min, washed with deionized water, and germinated on filter paper saturated with 200 µm CaCl2, in darkness at 25 °C for 3 d.

Experiment 1: growth experiment

Effect of Al, Ca and other divalent cations on root growth. Three seedlings of each cultivar, Oryza sativa L. ‘IR36’ (indica), ‘IR72’ (indica), ‘Kasalath’ (indica), ‘Oryzica Sabana 6’ (japonica × indica cross) and ‘Toyohatamochi’ (japonica), were transferred to a 2-L container containing the treatment solution under aeration. In Experiment 1, the solution with a low concentration of Ca (50 µm) was used as the control treatment to obtain a significant effect of cation application. All the cations were added as chloride salts in the present study. The treatments were: control (50 µm Ca), +Al treatment (20 µm Al, 50 µm Ca), +Ca treatment (500 µm Ca), +Sr treatment (450 µm Sr, 50 µm Ca), and +Ba treatment (450 µm Ba, 50 µm Ca). The pH of the solution was adjusted to 4·2 every day using 0·1 or 0·01 m HCl as appropriate. The change in pH between pH adjustments was less than 0·05. To evaluate the interaction between Ca and H+, root elongation at pH 5·0 (50 and 500 µm Ca) was also determined. Seedlings were grown for 6 d. Since the decrease in Ca concentration of the control solution during the treatment was less than 5 % of the initial value, the solutions were not replaced. The effect of treatments on root growth of each cultivar was evaluated by measuring the average relative root elongations (RRE) according to the formula: RRE = (RT − RT0)/(RC − RC0), in which RT and RT0 are the length of the longest root after and before the treatment, respectively, and RC and RC0 are the length of the longest root after and before the control treatment, respectively. Throughout this paper, experiments were carried out in a growth chamber (25 °C, dark) with three replications. In a preliminary experiment, we confirmed that the results under the dark conditions were the same as those under the light/dark conditions. We selected dark conditions because the data varied more widely among replications under the light/dark conditions.

Effect of Ca and Mg applications on Al, Sr, and Ba toxicities. Seedlings of five rice cultivars were transferred to 2-L containers containing treatment solution under aeration. The treatments were: control (50 µm Ca), +Al treatment (20 µm Al, 50 µm Ca), +Al+Ca treatment (20 µm Al, 500 µm Ca), +Al+Mg treatment (20 µm Al, 450 µm Mg, 50 µm Ca), +Sr treatment (450 µm Sr, 50 µm Ca), +Sr+Ca treatment (450 µm Sr, 500 µm Ca), +Sr+Mg treatment (450 µm Sr, 450 µm Mg, 50 µm Ca), +Ba treatment (450 µm Ba, 50 µm Ca), +Ba+Ca treatment (450 µm Ba, 500 µm Ca), and +Ba+Mg treatment (450 µm Ba, 450 µm Mg, 50 µm Ca). To evaluate the effect of a monovalent cation on Al toxicity, the +Al+Na treatment (20 µm Al, 1350 µm Na – as NaCl, same ionic strength as 450 µm CaCl2 − 50 µm Ca) was also applied. The effect of treatments on root growth of each cultivar was evaluated as described above.

Treatments similar to those conducted with rice seedlings were also tested on wheat seedlings. Wheat seeds (Triticum aestivum L. ‘Atlas 66’) were germinated for 1·5 d as described above. After germination, three seedlings of each cultivar were transferred to 2-L containers containing the treatment solution under aeration and grown for 3 d. The treatment and experimental conditions were the same as described for rice except that the Al concentration was 5 µm and the solution pH was 4·6.

Experiment 2: root staining

Pyrocatechol violet (PCV) produces a blue colour when a chelating complex is formed with Al (Watanabe et al., 1998; Britez et al., 2002). Therefore, PCV was used to visualize Al localization in roots of rice cultivars. Seedlings of the five cultivars were grown in 2-L containers containing 500 µm Ca at pH 4·2 for 3 d. Then, seedlings were transferred to 2-L containers containing 20 µm Al, 50 µm Ca or 20 µm Al, 500 µm Ca, and grown for 24 h. The roots after treatment were cut with a razor, washed with deionized water and stained with 0·2 g L−1 PCV in 25 g L−1 hexamine-NH4OH buffer (pH 6·2) for 5 min. After staining, the roots were washed with deionized water, and scanned with a scanner (GT-9300UF, Seiko Epson, Japan). The scanner was calibrated using preliminary samples, and scanning was carried out under the same conditions.

Methylene blue (MB), a cationic dye, is used for the rapid estimation of CEC of soils (Wang et al., 1996) or for the visualization of the surface negativity of plant root cells (Wagatsuma et al., 1988). In this experiment MB was used to visualize the CEC of rice roots. Seeds of the five rice cultivars were germinated as described above and transferred to a 2-L container containing 1000 µm Ca at pH 4·2 (Al-free). In order to fill cation exchange sites of the roots with Ca2+, a higher Ca concentration was applied. Seedlings were grown in a growth chamber for 3 d. The roots were cut with a razor, washed with deionized water, and then stained with 0·2 g L−1 MB for 1 min. After staining, the roots were washed with deionized water, and scanned.

Experiment 3: Al and Ca contents in root apices

Seedlings of five rice cultivars were transferred to 2-L containers containing treatment solution under aeration. The treatments were: control (50 µm Ca), +Al treatment (100 µm Al, 50 µm Ca), +Al+Ca treatment (100 µm Al, 500 µm Ca), and +Ca treatment (500 µm Ca). The pH in the solution was adjusted to 4·2 every day. Root apices (<0·5 mm) of seedlings grown for 3 d in a growth chamber were sampled. Root apices (50–70 apices) were homogenized in 1 n HCl and total Al and Ca contents were determined by atomic absorption spectrophotometry with a graphite furnace (Z-8000, Hitachi, Japan).

Experiment 4: change in aluminium tolerance of rice cultivars grown in increasing Ca concentrations

Seedlings of five rice cultivars were transferred to 2-L containers containing different levels of Ca (50, 200, 500, 1000, 2000 and 5000 µm) with or without 100 µm Al at pH 4·2, and grown for 4 d. Root elongation was expressed as a relative value to that in the control (−Al) treatment at each Ca level. In all treatments the concentration of Al was 100 µm and the pH was 4·2. For comparison, Al tolerance in ‘Toyohatamochi’ and ‘IR72’ was determined by growing these two varieties in 500 µm Ca, 4500 µm Na (NaCl) as a basal solution with an ionic strength equal to 2000 µm Ca.

Calculation of ionic activities

Ionic activities were calculated by a computer program developed by Wada and Seki (1994), and are shown in Table 1.

Table 1.

Ionic activities of Al and Ca in various solutions used in the present study

Ionic activities (µm)
20 µm Al
 100 µm Al
Al
 Ca
 Al
 Ca
50 µM Ca 13·4 46·2 62·2 44·4
200 µM Ca – – 57·9 171·1
500 µM Ca 11·0 416·2 52·7 407·2
1000 µM Ca – – 46·9 766·8
2000 µM Ca – – 39·6 1406·7
5000 µM Ca – – 28·8 2986·0
50 µM Ca + 450 µM Mg 11·0 41·6 – –
500 µM Ca + 4500 µM Na – – 39·6 350·6
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Statistics

Results were evaluated by analysis of variance and Fisher's LSD when significant (P ≤ 0·05) treatment effects were found.

RESULTS

Experiment 1: growth experiment

Effect of aluminium, calcium and other divalent cations on root growth. Al application inhibited root growth in all cultivars tested. The order of Al tolerance in the rice cultivars judged by RRE was: ‘Toyohatamochi’ > ‘Oryzica Sabana 6’ > ‘IR72’ > ‘IR36’ > ‘Kasalath’ (Fig. 1). Both Sr and Ba applications inhibited root growth. The order of cultivar tolerance to Sr and Ba corresponded to that of Al tolerance, except for ‘Kasalath’ with +Sr treatment (Fig. 1). Japonica (‘Toyohatamochi’) and the japonica × indica cross (‘Oryzica Sabana 6’) cultivars tended to be Al-tolerant compared to indica cultivars (‘IR36’, ‘IR72’ and ‘Kasalath’). Ca application stimulated root growth, especially in Al- (Sr- or Ba-) tolerant cultivars (Fig. 1). Root elongation was also enhanced at pH 5·0, especially in Al- (Sr- or Ba-) tolerant cultivars, and there was no additive effect of Ca application at pH 5·0 (Fig. 1). This result means that 50 µm Ca is sufficient for root elongation in rice and that Ca-induced stimulation of root elongation at low pH is due to the alleviation of H+ toxicity.

Fig. 1.

Fig. 1.

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Effect of Ca, Al, Sr and Ba application on root elongation in rice cultivars. Root elongation at pH 5 in 50 µm Ca and 500 µm Ca are also shown. Root elongation in each treatment is expressed relative to the value in the control treatment. Control = 50 µm Ca; +Ca = 500 µm Ca; +Al = 50 µm Ca, 20 µm Al; +Sr = 50 µm Ca, 450 µm Sr; +Ba = 50 µm Ca, 450 µm Ba (pH 4·2). Values are the means of three replicates. Bars indicates s.e. Different letters indicate statistically significant treatment effects (P ≤ 0·05).

Effect of Ca and Mg applications on Al, Sr, and Ba toxicities. Both Ca and Mg applications alleviated Al-induced growth inhibition in all cultivars, and the degree of alleviation was higher in Al-sensitive cultivars (Fig. 2A). Both +Ba and +Sr toxicities were alleviated by Ca application, but not by Mg application (Fig. 2B, C). In wheat, none of the cations, except for Al, inhibited root growth, but growth was stimulated by Ca and Ba treatment (Fig. 3A). Ca, Mg, and Ba had an ameliorative effect on Al toxicity (Fig. 3B).

Fig. 2.

Fig. 2.

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Effect of Ca and Mg applications on Al, Sr and Ba toxicities in rice cultivars. Root elongation in each treatment is expressed relative to the value in the control treatment. To evaluate the effect of monovalent cation on Al toxicity, the +Al+Na treatment was also applied. Values are the means of three replicates. (A) Al toxicity: control = 50 µm Ca; +Al = 50 µm Ca, 20 µm Al; +Al+Ca = 20 µm Al, 500 µm Ca; +Al+Mg = 50 µm Ca, 20 µm Al, 450 µm Mg; +Al+Na = 50 µm Ca, 20 µm Al, 1350 µm Na (pH 4·2). (B) Sr toxicity: control = 50 µm Ca; +Sr = 50 µm Ca, 450 µm Sr; +Sr+Ca = 450 µm Sr, 500 µm Ca; +Sr+Mg = 50 µm Ca, 450 µm Sr, 450 µm Mg (pH 4·2). (C) Ba toxicity: control = 50 µm Ca; +Ba = 50 µm Ca, 450 µm Ba; +Ba+Ca = 450 µm Ba, 500 µm Ca; +Ba+Mg = 50 µm Ca, 450 µm Ba, 450 µm Mg (pH 4·2). Bars indicates s.e. Fisher's LSD at P ≤ 0·05 is indicated (significant treatment effects at this level were found in ANOVA).

Fig. 3.

Fig. 3.

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Interactive effects of Al and divalent cation applications on root growth of wheat, ‘Atlas 66’. (A) Effect of cation treatment on root growth. (B) Effect of divalent cation treatment on Al toxicity. Root elongation in each treatment is expressed relative to the value in the control treatment. Values are the means of three replicates. Control = 50 µm Ca; +Ca = 500 µm Ca; +Al = 50 µm Ca, 5 µm Al; +Sr = 50 µm Ca, 450 µm Sr; +Ba = 50 µm Ca, 450 µm Ba; +Al+Ca = 5 µm Al, 500 µm Ca; +Al+Ca = 5 µm Al, 500 µm Ca; +Al+Mg = 50 µm Ca, 5 µm Al, 450 µm Mg; +Al+Sr = 50 µm Ca, 5 µm Al, 450 µm Sr; +Al+ Ba = 50 µm Ca, 5 µm Al, 450 µm Ba (pH 4·6). Bars indicates s.e. Fisher's LSD at P ≤ 0·05 is indicated (significant treatment effects at this level were found in ANOVA).

Experiment 2: root staining

Only root apices were stained with PCV. The degree of staining was remarkable in indica cultivars (‘IR36’, ‘IR72’ and ‘Kasalath’) and corresponded to the order of Al tolerance (Figs 1, 4A). Ca application decreased the staining intensity in all cultivars (Fig. 4A). Root tips of cultivars grown without Al also stained deeply with MB with a slightly lighter intensity in the Al-tolerant line ‘Toyohatamochi’ (Fig. 4B). Interestingly, in indica cultivars root slime was found at the tips, as shown by the more intense MB staining pattern.

Fig. 4.

Fig. 4.

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Roots of rice cultivars stained with (A) PCV and (B) MB. Before PCV staining, seedlings were grown with 50 µm Ca, 20 µm Al or 500 µm Ca, 20 µm Al at pH 4·2 for 24 h. Before MB staining, seedlings were grown with 1000 µm Ca at pH 4·2 (Al-free) for 3 d.

Experiment 3: Al and Ca contents in root apices

The total Al content in root apices treated with +Al was higher in ‘IR36’ than in ‘Toyohatamochi’, and decreased as a result of Ca application, most remarkably in ‘Toyohatamochi’ (Fig. 5). The total Ca content in root apices did not change as much as the total Al content under these conditions. Root tips of ‘IR36’ had a slightly decreased Ca concentration after +Al treatment that could be recovered by Ca application (Fig. 5). The total Ca content in root apices of ‘IR36’ was significantly higher than that of ‘Toyohatamochi’ in the control treatment.

Fig. 5.

Fig. 5.

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Al and Ca contents in root apices (<0·5 mm) of rice cultivars, ‘Toyohatamochi’ (Al-tolerant) and ‘IR36’ (Al-sensitive), after treatment (3 d, pH 4·2). Control = 50 µm Ca; +Ca = 500 µm Ca; +Al = 100 µm Al, 50 µm Ca; +Al+Ca = 100 µm Al, 500 µm Ca. Bars indicates s.e. Fisher's LSD at P ≤ 0·05 is indicated (significant treatment effects at this level were found in ANOVA).

Experiment 4: change in aluminium tolerance of rice cultivars grown in increasing Ca concentrations

At low Ca (≤500 µm), Al tolerance in indica cultivars was obviously lower than that of japonica cultivars. However, the differences in Al tolerance between indica and japonica cultivars became small with increasing concentrations of Ca in the medium. At high Ca concentration (≥2000 µm) there was almost no difference in RRE between indica and japonica cultivars (Fig. 6). The effect of Ca was mimicked by treatment with Na at the same ionic strength (diamond symbols in Fig. 6).

Fig. 6.

Fig. 6.

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Effect of increased levels of Ca in the medium on Al toxicity in rice cultivars. Root elongation is expressed as a relative value to that in the control (−Al) treatment at each Ca level (50, 200, 500, 1000, 2000, and 5000 µm). Bars indicates the s.e. (n = 6). Fisher's LSD at P ≤ 0·05 is indicated at each Ca level (significant treatment effects at this level were found in ANOVA). Open diamonds and closed diamonds indicate ‘Toyohatamochi’ and ‘IR72’, respectively, in 500 µm Ca, 4500 µm Na (NaCl) as a basal solution that has an ionic strength equal to 2000 µm Ca.

DISCUSSION

In general, Sr and Ba show toxicity only in extremely high concentrations (Wallace and Romney, 1971; Davis et al., 1978). In some cases these elements may show beneficial effects. Root elongation of wheat was stimulated by 450 µm Ca and Ba, not affected by 450 µm Sr, and inhibited by 5 µm Al (Fig. 3A). Ca- and Ba-induced stimulation of root elongation seems to be caused by the alleviation of H+ toxicity under low pH conditions (Koyama et al., 2001). On the other hand, not only Al but also Sr and Ba inhibited root elongation in rice. Interestingly, the order of tolerance to Sr or Ba corresponded closely to that of Al, namely tolerant in japonica lines and sensitive in indica cultivars (Fig. 1). Ca application alleviated this growth inhibition in all cultivars, with the degree of alleviation higher in sensitive cultivars (Fig. 2A). Since Sr and Ba are in the same group of elements as Ca, it is expected that competition with Ca absorption and/or displacement of Ca from critical sites in the root apoplast participate in the toxicity of these elements. Therefore, if the mechanism of Al toxicity is the same as those for Sr or Ba toxicity, then the Ca2+-displacement hypothesis might be operational in rice cultivars. Although Mg application did not affect Sr or Ba toxicity, it alleviated Al toxicity to the same extent as Ca application (Fig. 2). Moreover, Na application at the same ionic strength as the Ca application also alleviated Al toxicity in rice cultivars (Fig. 2). This result indicates that Ca may have a specific, irreplaceable role in Sr and Ba toxicities but not in Al toxicity.

When seedlings exposed to Al for 24 h were stained with PCV, root apices were stained deeply in Al-sensitive cultivars, showing higher Al accumulation (Fig. 4A). When the seedlings were grown with Al for 3 d as well, the Al content in root apices of ‘Toyohatamochi’ (Al-tolerant) was much lower than that of ‘IR36’ (Al-sensitive) (Fig. 5). In common with results in other plant species, for example wheat (Polle et al., 1978) and Brachiaria sp. (Wenzl et al., 2001), Al tolerance in rice seems to be negatively correlated with Al content in root tips. Although Al content in root apices was significantly less as a result of Ca application (Figs 4, 5), the Ca content of the tissue was hardly affected (Fig. 5). This result also refutes the Ca2+-displacement hypothesis in rice. Discovering the reason why Al content is decreased by Ca application (and probably other cations) without displacement of Al will be an important step leading to the elucidation of the mechanisms of Al toxicity in rice.

Although the results obtained from this study do not support the Ca2+-displacement hypothesis, analysis of the interaction of Al with cations, including Ca, in the medium will be the key to solving the mechanism of Al toxicity in rice. Figure 6 shows the change in Al tolerance of rice cultivars grown in increasing Ca concentrations. Whereas Al tolerance in indica cultivars was obviously lower under low Ca conditions, the difference in Al tolerance between indica and japonica cultivars disappeared under high Ca conditions. Since the effect of Ca was substituted by Na (diamond symbols in Fig. 6), it is strongly suggested that the primary mechanism of Al toxicity in rice cultivars changes depending on the ionic strength of the medium. Recently, Pintro and Taylor (2004) also pointed out that the ionic strength in media should be considered carefully to simulate natural soil solutions when screening for Al tolerance. Although the high ionic strength decreased the activities of Al in solution (Table 1), Al activity in 20 µm Al and 50 µm Ca – a treatment in which obvious differences in Al tolerance between japonica and indica cultivars are found (Fig. 1) – is lower than that in the solution containing 100 µm Al and ≥1000 µm Ca, in which a significant difference among cultivars was observed irrespective of cultivar type (Fig. 6). Therefore, factor(s) other than Al activity, probably concentrations of cations in media are important, and different electrochemical characteristics of root tip cells, such as the surface negativity of the plasma membrane (Wagatsuma and Akiba, 1989) or characteristics of cell walls (Masion and Bertsch, 1997), may account for the difference in Al tolerance between japonica and indica cultivars. Ca content in root tips of ‘IR36’ was significantly higher than that of ‘Toyohatamochi’ (Fig. 5), suggesting the contribution of root-tip CEC to Al tolerance in rice cultivars. The root slime with negative charges found at the root tips of indica cultivars could provide a clue to solve this problem (Fig. 4).

CONCLUSIONS

In conclusion, the Ca2+-displacement hypothesis is not a suitable model to describe the mechanism of Al toxicity in rice cultivars. However, concentration of cations, including Ca, remarkably affects Al tolerance in rice cultivars; more specifically, Al tolerance in indica cultivars decreases remarkably under low ionic strength conditions. Screening for Al tolerance in a medium with high ionic strength may underestimate the difference of Al tolerance in rice cultivars grown in highly weathered, acidic soils with low exchangeable basic cations.

Acknowledgments

Part of this study was financially supported by the Akiyama Foundation of Japan.

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