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First published online April 28, 2006; 10.1104/pp.105.076497 Plant Physiology 141:674-684 (2006) © 2006 American Society of Plant Biologists Phosphorus and Aluminum Interactions in Soybean in Relation to Aluminum Tolerance. Exudation of Specific Organic Acids from Different Regions of the Intact Root System1,[W]Root Biology Center, South China Agricultural University, Guangzhou 510642, China (H.L., H.W., X.W., X.Y.); and United States Plant, Soil, and Nutrition Laboratory, United States Department of Agriculture Agricultural Research Service, Cornell University, Ithaca, New York 14853 (J.S., L.V.K.)
Aluminum (Al) toxicity and phosphorus (P) deficiency often coexist in acid soils that severely limit crop growth and production, including soybean (Glycine max). Understanding the physiological mechanisms relating to plant Al and P interactions should help facilitate the development of more Al-tolerant and/or P-efficient crops. In this study, both homogeneous and heterogeneous nutrient solution experiments were conducted to study the effects of Al and P interactions on soybean root growth and root organic acid exudation. In the homogenous solution experiments with a uniform Al and P distribution in the bulk solution, P addition significantly increased Al tolerance in four soybean genotypes differing in P efficiency. The two P-efficient genotypes appeared to be more Al tolerant than the two P-inefficient genotypes under these high-P conditions. Analysis of root exudates indicated Al toxicity induced citrate exudation, P deficiency triggered oxalate exudation, and malate release was induced by both treatments. To more closely mimic low-P acid soils where P deficiency and Al toxicity are often much greater in the lower soil horizons, a divided root chamber/nutrient solution approach was employed to impose elevated P conditions in the simulated upper soil horizon, and Al toxicity/P deficiency in the lower horizon. Under these conditions, we found that the two P-efficient genotypes were more Al tolerant during the early stages of the experiment than the P-inefficient lines. Although the same three organic acids were exuded by roots in the divided chamber experiments, their exudation patterns were different from those in the homogeneous solution system. The two P-efficient genotypes secreted more malate from the taproot tip, suggesting that improved P nutrition may enhance exudation of organic acids in the root regions dealing with the greatest Al toxicity, thus enhancing Al tolerance. These findings demonstrate that P efficiency may play a role in Al tolerance in soybean. Phosphorus-efficient genotypes may be able to enhance Al tolerance not only through direct Al-P interactions but also through indirect interactions associated with stimulated exudation of different Al-chelating organic acids in specific roots and root regions.
Acid soils comprise up to 50% of the world's potentially arable land and thus are a significant limitation to crop production worldwide (von Uexküll and Mutert, 1995  ). On most acid soils, there are several limiting factors for plant growth, including toxic levels of aluminum (Al), manganese, and iron (Fe), as well as deficiencies of some essential elements, such as phosphorus (P), nitrogen, potassium (K), calcium (Ca), magnesium, and some micronutrients (Kochian et al., 2004). Among these constraints, Al toxicity and P deficiency are the most important due to their ubiquitous existence and overwhelming impact on plant growth (Kochian et al., 2004).
Aluminum toxicity limits plant growth mainly through its adverse effects on root growth and development. Under acidic soil conditions, active, phytotoxic forms of Al are released to the soil solution to levels that can inhibit root growth and damage roots (Foy, 1984
Low-P availability is another important limiting factor to plant growth in acid soils. In most humid tropical and subtropical regions where acid soils prevail, warm and moist conditions result in weathered soil types (mostly Ustisols, Oxisols), in which free Fe and Al oxides bind native and applied P into forms unavailable to plants (Barber, 1995
Although many studies have been conducted on plant Al tolerance and P efficiency on acid soils, Al toxicity and P deficiency are almost always studied separately as independent factors (Foy, 1988
Relatively few studies have been done to investigate Al and P interactions in plants. Tan and Keltjens (1990)
We have recently established an applied core collection of soybean germplasm and identified materials with varying growth performance and yield potential on the acidic low-P soils of South China (Zhao et al., 2004
Al and P Interactions on Soybean Root Growth in Homogeneous Nutrient Solution
In this study, four soybean genotypes were used that we previously have shown to differ in P efficiency (the ability to tolerate P deficiency stress; Zhao et al., 2004
Under these homogenous low-P conditions, no significant genotypic differences in Al tolerance were observed among the four genotypes that were previously shown to contrast under low-P and acidic field conditions (Fig. 1). Phosphorus addition to the homogeneous hydroponic media significantly increased Al tolerance of the four soybean genotypes as indicated by relative taproot lengths, and the root growth inhibition by Al toxicity was significantly alleviated at the highest P level (320 µM P), thus demonstrating a significant Al-by-P interaction (Fig. 2A ).
Moderate but statistically significant genotypic differences in Al tolerance were observed among the four soybean genotypes when the P level in the hydroponic media was increased from 0 to 80 µM, in that the two P-efficient soybean genotypes exhibited higher levels of Al tolerance than did the P-inefficient varieties. This differential Al tolerance disappeared at the highest P level employed (320 µM P; Fig. 2A). The observation of differential Al tolerance was also supported by scanning electron micrographs of the root apices, which showed that roots exposed to low-P media plus Al were severely damaged, whereas exposure of roots to increasing P levels plus Al exhibited far fewer symptoms of root damage less affected by Al, particularly for the two P-efficient genotypes (Fig. 2B). It should be noted in Figure 2B that at the highest P level employed (320 µM P), a greater degree of root damage was still seen in the two P-inefficient genotypes. However, at this P level there was only a small degree of Al inhibition of root growth. Thus, it appears that symptoms of Al-induced physical damage to roots does not necessarily correlate with Al-induced root growth inhibition. Phosphorus supplementation of the hydroponic media also significantly decreased Al accumulation in the root tips (the terminal 2 cm of the root) as indicated by both hematoxylin staining and direct quantification of root Al content using inductively coupled plasma (ICP) emission spectroscopy (Fig. 3, A and B ). In accordance with the findings for relative root growth in Figure 2, the two P-efficient soybean genotypes accumulated less Al in the root apices than did the P-inefficient varieties under P supplementation (Fig. 3, A and B), indicating that Al exclusion from the root tips might be an Al tolerance mechanism that is influenced by increased plant P availability and nutrition.
Root Organic Acid Exudation in Homogeneous Nutrient Solution Citrate and malate were the two major organic acids induced by Al toxicity and/or low-P availability in the homogenous collection system, while oxalate appeared to be mainly induced by P deficiency (Fig. 4 ). Citrate exudation was strongly induced by Al toxicity, but much less so by P deficiency (Fig. 4, A–D). Al-induced citrate exudation was greatly decreased when roots were also grown on high-P levels, indicating that there is a clear Al-by-P interaction regarding root citrate exudation. It should be noted that this was not simply an effect of chelation of exogenous Al by P, as the nutrient solutions were designed to maintain the same free Al3+ activity as the level of P in the nutrient solution was increased, using the speciation program GEOCHEM-PC to calculate Al3+ activities in solution. Interestingly, the rate of Al-activated root citrate exudation increased from 6 to 24 h of Al exposure, and then maintained a relatively high constant level of exudation over the subsequent time points (48 and 72 h). On the other hand, the relatively low levels of citrate exudation induced by low-P status were only seen over the first 6 h of the exudation period. This demonstrates that the Al-activated citrate exudation is a relatively long-term response while low-P-induced citrate exudation is transient.
Similar to citrate exudation, malate exudation was induced by both Al and low P, but its pattern was different from that of citrate exudation. For example, the low-P treatment elicited a significant malate exudation, which completely disappeared at high P (320 µM; Fig. 4, E–H). Malate exudation was also activated by Al exposure. As was seen for citrate release, this response was greatly reduced under high-P treatment, again indicating there is a significant Al-by-P interaction on root malate exudation. Unlike citrate and malate release, oxalate exudation was activated primarily by P deficiency, and the relative rate of P deficiency-induced oxalate exudation was much higher than the rates of citrate and malate exudation induced by low-P status (Fig. 4, I–L). Interestingly, Al-activated oxalate exudation was detectable in the high-P plants over the first 6 h of exudation, particularly for the two P-efficient genotypes, and then disappeared, indicating this Al-activated oxalate exudation is transient.
The specially designed Plexiglas chamber depicted in Figure 5 was used to isolate the solution bathing the intact root system into two compartments, upper and lower, where the upper chamber housed the first approximate 6 cm of the taproot and associated lateral roots, and the lower chamber housed the rest of the taproot. Furthermore, root exudation of organic acids was collected specifically from the terminal approximately 1.5 cm of the taproot, using a Plexiglas ring that straddled the root and isolated the root apex from the rest of the root system. This system was used to mimic the soil conditions for a low-P acid soil, such that ±P treatments were applied only to the upper chamber, and Al exposure under –P conditions was imposed in the lower chamber.
In this heterogeneous nutrient solution system, soybean taproot growth for all four soybean genotypes was significantly inhibited by Al toxicity under –P conditions in both chambers (Fig. 6, A and C ). When the solution P concentration was increased in the upper compartment, the Al tolerance measured as relative taproot growth was greatly improved specifically for the two P-efficient genotypes over the first 24 h of the experiment. This finding was further confirmed by hematoxylin staining, which showed that the two P-efficient genotypes accumulated less Al than the two P-inefficient genotypes when high P was applied to the upper compartment (Fig. 6, B and D). At the later time points (48 and 72 h), this improved Al tolerance disappeared, indicating that, under the conditions imposed by these experiments, localized P supply could only transiently increase Al tolerance in the P-efficient genotypes.
As was done for roots homogeneously exposed to Al and/or different P regimes, organic-acid exudation specifically from the taproot apex was studied under the stratified conditions of P and Al exposure. As seen in Figure 7 (A–D) , citrate exudation from the root tip was strongly activated by Al exposure in the lower chamber, when the roots in the upper chamber were grown under both ±P conditions. The major difference between the low- versus high-P treatment in the upper chamber was the rate of Al-activated citrate exudation at the earliest time point (6 h). Here, the high-P treatment imposed on the upper portion of the root system resulted in a much larger Al-activated citrate release from the taproot apex residing in the lower chamber. No significant genotypic differences were observed in Al-activated citrate exudation from root tips among the four soybean genotypes, suggesting that, under these conditions that more closely mimic the real-world situation, root citrate exudation might not be a major mechanism of soybean Al tolerance, at least for the taproot.
The major difference in root malate exudation between this experiment and the one depicted in Figure 4 for the homogenous treatments of roots was that high-P status in the upper chamber dramatically stimulated Al-activated malate release from the taproot, at least for the early stages of the experiment (6 and 24 h; Fig. 7, E–H). Furthermore, the two P-efficient soybean genotypes had significantly higher malate exudation from the root tips over the first 6 h (Fig. 7, E–H), indicating that the increased root tip growth in the first 24 h might be attributed to the higher rates of taproot apical malate exudation that was stimulated by providing more P to the upper portions of the root system. In comparing the data for taproot tip Al-activated malate exudation in Figure 7, G and H, with whole root Al-activated malate exudation in Figure 4, G and H, it is not clear if the Al-activated malate exudation from the whole root system under high-P nutrition in Figure 4 is primarily due to the taproot tip malate exudation depicted in Figure 7. However, as shown in Supplemental Figure 2 where Al-activated root malate exudation was measured from all three compartments (upper compartment, lower compartment, and taproot tip) under conditions where the upper compartment received high P, it is clear that high-P status in the upper chamber dramatically stimulated malate release from the whole root system for the first 6 h of the experiment, especially in the two P-efficient genotypes. Furthermore, almost all of the malate was secreted from the taproot tips in response to Al. With regard to oxalate exudation from the taproot apex, this release was only induced by low-P status, as was also seen for exudation from the entire root system. As seen in Figure 7, I to L, high rates of root tip oxalate exudation were found in all four treatments, indicating that the low-P status of the chamber where the taproot tip grew was the primary factor triggering root tip oxalate exudation.
Soybean Al Tolerance as Influenced by Changes in P Status
In the literature, plant Al tolerance is commonly determined by measuring the relative root growth in a simple salt solution, such as CaCl2 or CaSO4, in the absence or presence of different Al concentrations (Kinraide et al., 1985
Because of the complexities of Al solution chemistry, particularly with regards to its interactions with phosphate in solution, it is critical to model the solution chemistry with a computer speciation program, such as the GEOCHEM-PC used here (Parker et al., 1995
Al toxicity and P deficiency often coexist in acid soils, and therefore the relative ranking of Al tolerance in plants may be affected by P and Al interactions. This was the case in our study. The four soybean genotypes differing in P efficiency did not significantly differ in Al tolerance when no or very low levels of P were included in the homogeneous nutrient solution (Fig. 2). However, when higher levels of P were included in the nutrient solution, the Al tolerance of all the four soybean genotypes was significantly increased, with basically no Al toxicity symptoms seen at the highest solution P concentration employed (320 µM; Fig. 2). Under these conditions, evidence for some differential Al tolerance was seen, as the two P-efficient genotypes appeared to be more Al tolerant than the P-inefficient genotypes. This agrees with some previous findings suggesting that P had positive effects with regard to ameliorating Al tolerance (Gaume et al., 2001
It could be assumed that plants that perform well on low-P acid soils should possess root systems that are both Al tolerant and P efficient. But this is not necessarily the case in many soils that are heterogeneous with regard to distribution of Al and P in the soil horizon, in which case different root type may respond differently to Al toxicity and low P. In this study, we used a divided root chamber system that allowed us to maintain a localized supply of P and/or Al to simulate the actual growth conditions in low-P acid soils. We found that soybean taproot growth of the two P-efficient genotypes was less affected by Al toxicity (more Al tolerant) than the two P-inefficient genotypes in experiments where high P was supplied to the roots in the upper horizon, and Al toxicity and P deficiency was imposed in more deeply situated roots. This result is consistent with what we found in field studies with soybean, where P-efficient soybean genotypes had greater growth of shallow roots in the upper soil horizons where soil pH and P levels are higher, while the taproot grew more effectively in more acidic, low-P subsoil, compared with P-inefficient genotypes (Zhao et al., 2004
One obvious possible explanation for the greater taproot Al tolerance of the P-efficient genotypes in a soil with a heterogeneous distribution of Al and P is that these genotypes may more effectively acquire P from the upper soil horizons and thus maintain a more optimal P nutrition, which could result in more robust root function. It was recently suggested that P could help ameliorate Al tolerance not only through Al complexation and possible precipitation of Al in the rhizosphere, but also through Al-P interactions in the root apoplast or even at the root-cell plasma membrane (Zheng et al., 2005
Organic acid exudation is considered as a major mechanism of Al tolerance and P efficiency in certain plant species (Ma et al., 2001 On the other hand, organic acid exudation patterns were quite different in the divided root chamber system that employed a stratified distribution of Al and P in the root bathing solution. Although the same three organic acids (i.e. citrate, malate, and oxalate) were detected in root exudates in the various treatments applied in this system, their exudation patterns were very different from those in the homogeneous solution system. For example, Al-activated citrate exudation from the taproot apex was significantly increased by localized supply of P to the upper portion of the root system over the first 6 h, indicating that alterations in P nutrition may play a role in soybean Al tolerance mediated by citrate exudation (Fig. 7, A–D). It is quite likely that the protection of roots from Al during their early stages of development is important to their long-term growth and survival. Therefore, the increased organic acid exudation observed during the early time points of root exposure to Al could contribute to Al tolerance of soybean. In our divided root system experiments, genotypic differences in organic acid exudation in response to localized P and Al supply were observed that were not seen when the entire root system was exposed to the same Al and P treatments. In comparing Figures 4 and 7, it is seen that the two P-efficient genotypes secreted approximately the same amount of citrate but much more malate from the taproot apex when the lateral roots in the upper portion of the root system were supplied with higher levels of P and Al toxicity was imposed to the terminal 6 cm of the taproot. These findings suggest that improved plant P nutrition, which is linked to genotypic differences in P efficiency, may play a role in enhanced Al toxicity exhibited by more deeply penetrating taproots. In conclusion, our results demonstrate that P efficiency may play a role in Al tolerance in soybean. Phosphorus-efficient genotypes may be able to enhance Al tolerance not only through direct Al-P interactions but also through indirect interactions associated with stimulated exudation of different Al-chelating organic acids in specific roots and root regions, which in turn enhances plant tolerance to Al toxicity.
Plant Materials
Four soybean (Glycine max L. Merr.) genotypes contrasting in their adaptability to low-P soil conditions and acidic soils were selected from an applied core collection of soybean germplasm (Zhao et al., 2004
Surface-sterilized seeds of the four soybean genotypes were germinated on paper towels moistened with one-half-strength modified Hoagland nutrient solution for 3 d at 25°C. The nutrient solution contained the following macronutrients (in mM): Ca, 2.0; K, 3.0; magnesium, 0.5; NO3–, 7.0; and SO42–, 0.5, and micronutrients (in µM): Fe-EDTA, 12.5; manganese, 1.0; Zn, 1.0; Cu, 1.0; NH4+, 0.25; MoO4–, 0.25; H3BO3, 12.5; and Cl–, 25. Aluminum treatments were imposed after this 3-d period by replacing the nutrient solution with the same solution containing Al3+ as AlCl3. Five Al3+ activity levels were employed, ranging from 0, 15, 30, 45, or 60 µM Al3+. The desired Al3+ activities were estimated using the GEOCHEM-PC speciation software (Parker et al., 1995
Sterilized seeds of the four soybean genotypes were germinated as described above with one-half-strength modified Hoagland nutrient solution with five different P treatments, P1, P2, P3, P4, and P5, which contained 0, 20, 40, 80, or 320 µM P as KH2PO4, respectively, for 3 d at 25°C. After 3 d of germination, seedlings were transplanted into 8-L polyethylene containers with the specific Al and P treatments. There were six treatments in total, including P1 + Al, P2 + Al, P3 + Al, P4 + Al, and P5 + Al, in which 0, 20, 40, 80, and 320 µM P were added as KH2PO4, respectively, together with 38 µM Al3+ activity based on the results from the above initial Al tolerance characterization experiment. An additional treatment without P and Al addition (P1-Al) was used as a control. The solution was well aerated and the pH was maintained at 4.2 with daily additions of dilute HCl. After 3 d of Al treatment, the morphology of the root apex from the taproot under P1-Al, P1 +Al, and P5 +Al treatments was documented using scanning electron microscopy, then plants were harvested and the taproot length was measured with a ruler as the indicator of Al tolerance.
Sterilized seeds of the four soybean genotypes were germinated as described above. Seedlings were transplanted into 8-L polyethylene containers with the specific Al and P treatments 3 d after germination. There were four treatments in total, including two P levels (0 and 320 µM P added as KH2PO4) and two Al3+ activities (0 and 38 µM Al3+ added as AlCl3). At 0, 24, 48, and 72 h after treatment, two plants for each treatment were then transferred into 50-mL sterilized plastic tubes filled with 45 mL of exudation media to collect organic acids exuded from the roots for 6 h. The exudation media consisted of 4.3 mM CaCl2, plus the Al and P treatments as described above. The pH of exudation media was adjusted to 4.5 with HCl or KOH. After collection, plants were carefully taken out of the tubes and put back into the polyethylene containers for further growth. After the last collection of root exudates, the first 2 cm of the taproot from half of the tested plants was stained by hematoxylin solution for 1 h as described by Delhaize et al. (1993b)
All the root exudate samples collected were passed through a silver cartridge (OnGuardII Ag; Dionex) to remove excess Cl–, then mixed with a cation-exchange resin (100:1, v/w) to remove cations. The mixtures were centrifuged at 1,000g for 3 min at 4°C. The supernatants were used for organic acid determination with a capillary electrophoresis system (P/ACE 5510; Beckman Instruments) controlled by a Pentium II computer interfaced via PACE 1.2.1 software (Beckman Instruments). The background electrolyte cleaning and organic acid separation method were as described by Piñeros et al. (2002)
Following germination in paper towels for 3 d, plants were transplanted into the specially designed divided root chambers (Fig. 5). One plant was transplanted into each chamber, and the terminal 6 cm of the taproot was isolated from the rest of the root system by a Plexiglas block that straddled the taproot via a notch cut into the Plexiglas. For collection of root exudates, an additional Plexiglas ring with a notch cut into its base was used to isolate the terminal 1.5 cm of the taproot for exudate collection. The treatment solutions within the three compartments were isolated from each other using silicon grease to make a watertight seal of each divider with the chamber base. The root tip compartment was filled with 10 mL of collection solution for root exudates. After root exudates were collected, each compartment was refilled with the same volume of treatment solutions. There were four treatments: 1, LP, LP – Al, which was –P solution without Al in both the upper and lower chambers as well as the root exudate chamber; 2, LP, LP + Al, which was –P media without Al in the upper chamber, and –P media plus 38 µM Al3+ (activity) in the lower and root exudate chambers; 3, HP, LP – Al, which was 320 µM P without Al in the upper chamber, and –P media without Al in the lower and root exudates chambers; and 4, HP, LP + Al, which was 320 µM P without Al in the upper chamber, and –P media plus 38 µM Al3+ in the lower and root exudate chambers. Relative root tip growth (%) was determined as the percentage of taproot growth within the Plexiglas ring at low P and high P with Al addition relative to that without Al addition at a given P level. Root exudate solutions were collected over a 6-h time period at 0, 24, 48, and 72 h after transplanting. The organic acids in the root exudate solutions were determined as described above. Taproot growth was measured at 0, 24, 48, and 72 h after treatment and before root exudate collection.
Another short-term experiment was carried using the same divided root growth chamber above for Al staining with hematoxylin. After 24 h of Al treatment, the first 2 cm of the taproot was stained by hematoxylin solution for 1 h as described by Delhaize et al. (1993b)
All of the data were analyzed statistically using Microsoft Excel 2000 (Microsoft) for calculating mean and SE and SAS (SAS Institute) for ANOVA.
We thank Eric Craft and Randy Clark for technical help and Drs. Vera M. Carvalho Alves, Jonathan Lynch, Rebecca Nelson, and Hong Shen for valuable discussions. Received December 29, 2005; returned for revision March 26, 2006; accepted April 17, 2006.
1 This work was supported by grants from National Key Basic Research Special Funds of China (grant no. 2005CB120902), the McKnight Foundation Collaborative Crop Research Program and the National Natural Science Foundation of China (grants to X.Y. and H.L.), and by grants from the McKnight Foundation Collaborative Crop Research Program and U.S. Department of Agriculture National Research Initiative (grant no. 2001–35301–10647 to L.K.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Leon V. Kochian (lvk1{at}cornell.edu).
[W] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.076497. * Corresponding author; e-mail lvk1{at}cornell.edu; fax 607–255–2459.
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Plant Physiol 138: 297–303 This article has been cited by other articles:
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