AOBPreview published online on August 29, 2008
Annals of Botany, doi:10.1093/aob/mcn166
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Phosphorus Enhances Al Resistance in Al-resistant Lespedeza bicolor but not in Al-sensitive L. cuneata Under Relatively High Al Stress
1 State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China
2 Graduate University of Chinese Academy of Sciences, Beijing 100049, China
* For correspondence. E-mail rfshen{at}issas.ac.cn
Received: 31 March 2008 Returned for revision: 22 May 2008 Accepted: 9 July 2008
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: Aluminium (Al) toxicity and phosphorus (P) deficiency often co-exist in acidic soils and limit crop production worldwide. Lespedeza bicolor is a leguminous forage species that grows very well in infertile, acidic soils. The objective of this study was to investigate the effects of Al and P interactions on growth of Lespedeza and the distributions of Al and P in two different Al-resistant species, and to explore whether P can ameliorate the toxic effect of Al in the two species.
Methods: Two species, Lespedeza bicolor and L. cuneata, were grown for 30 d with alternate Al and P treatments in a hydroponics system. Harvested roots were examined using a root-system scanner, and the contents of Al, P and other nutrient elements in the plants were determined using inductively coupled plasma-atomic emission spectroscopy (ICP-AES). Haematoxylin staining was used to observe the distribution of Al in the roots of seedlings. After pre-culture with or without P application, organic acids in the exudates of roots exposed to Al were held in an anion-exchange resin, eluted with 2 M HCl and then analysed using high-performance liquid chromatography (HPLC).
Key Results Lespedeza bicolor: exhibited a stronger Al resistance than did L. cuneata; Al exclusion mechanisms may mainly be responsible for resistance. P application alleviated the toxic effect of Al on root growth in L. bicolor, while no obvious effects were observed in L. cuneata. Much less Al was accumulated in roots of L. bicolor than in L. cuneata after P application, and the P contents in both roots and shoots increased much more for L. bicolor than for L. cuneata. Lespedeza bicolor showed a higher P/Al ratio in roots and shoots than did L. cuneata. P application decreased the Al accumulation in root tips of L. bicolor but not in L. cuneata. The amount of Al-induced organic acid (citrate and malate) exudation from roots pre-cultured with P was much less than from roots without P application; no malate and citrate exudation was detected in L. cuneata.
Conclusions: P enhanced Al resistance in the Al-resistant L. bicolor species but not in the Al-sensitive L. cuneata under relatively high Al stress, although P in L. cuneata might also possess an alleviative potential. Enhancement of Al resistance by P in the resistant species might be associated with its more efficient P accumulation and translocation to shoots and greater Al exclusion from root tips after P application, but not with an increased exudation of organic acids from roots.
Key words: Lespedeza bicolor, L. cuneata, Al toxicity, Al resistance, root morphology, phosphorus
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Normal plant growth in acidic soils can be limited by many chemicals or the interactions among them (Marschner, 1991). Aluminium (Al) toxicity and phosphorus (P) deficiency are recognized as the major constraints on crop productivity (Kochian et al., 2004; Fukuda et al., 2007). Although an improved crop production in acidic soils is possible with lime application, such application is neither economical for all farmers nor a thorough method for correcting subsoil acidity (Kochian et al., 2005). Phosphate fertilizers are often applied in acid soil areas to decrease Al activity and increase crop production. However, further exploration of the mechanisms of Al–P interactions in plants is still needed. On the other hand, not all species or genotypes express the same traits for Al toxicity and P deficiency (Marschner, 1991). Hence, a reasonable alternative or supplemental approach is to select and breed plant genotypes having greater resistance to these stresses (Foy, 1988).
Genotypic differences in Al resistance have been found in many crops including wheat (Delhaize et al., 1993; de Sousa, 1998; Kariuki et al., 2007), triticale (Oettler et al., 2000; Kim et al., 2001), buckwheat (Yang et al., 2005), barley (Zhao et al., 2003), rice (Sivaguru and Paliwal, 1994) and rye (Aniol et al., 1980; Gallego and Benito, 1997). Lespedeza is a considerably Al-resistant plant (Campbell et al., 1991), but genetic differences in Al resistance still exist (Dong et al., 2008). Previous studies have suggested that Al resistance mechanisms of Lespedeza are associated with the exudation of malic and citric acids under Al stress (Dong et al., 2008). However, little information is available about Al and P interactions in different Lespedeza species.
Although many studies have been conducted on Al resistance and P efficiency of plants in acidic soils, there are few studies on Al and P interactions in plants (Liao et al., 2006). McCormick and Borden (1972) found, using the molybdenum blue technique, that the Al–P interaction appeared to be associated with the cell wall and the outside of the cytoplasmic membrane of epidermal and cortical cells in barley. Tan and Keltjens (1990a) reported that an increase in the P concentration played a role in ameliorating Al phytotoxicity, possibly through improving root development and nutrient uptake. In addition, the toxic effect of Al on plant growth was alleviated with increasing P contents in roots. Al resistance in a resistant cultivar was associated with a higher Al immobilization ability in the presence of P in root tissues as compared with an Al-susceptible cultivar (Gaume et al., 2001). As proposed by Zheng et al. (2005), Al resistance of buckwheat involves both the secretion of oxalic acid from root apices and the precipitation of Al by P in the root apoplast. Liao et al. (2006) provided evidence that P-efficient genotypes might be able to enhance Al resistance not only through direct Al–P interactions but also by indirect interactions associated with stimulated exudation of different Al-chelating organic acids in specific roots and root regions. Therefore, the relationship of Al and P is ubiquitous and may vary in different crops. However, for Lespedeza species, the effect of the interaction of P and Al in roots on alleviating Al toxicity may be another potential mechanism in addition to the mechanism of organic acid efflux. In the current study, root morphology, nutrient elements and organic acid exudation analyses were carried out to aid in the understanding of the the relationship of Al and P under hydroponic conditions in two Lespedeza species under Al stress.
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MATERIALS AND METHODS |
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Plant materials and growth conditions
Lespedeza bicolor (Turcz. ‘Jiangxi’) seeds were collected from Jiangxi Province, China. Seeds were surface softened in 98 % H2SO4 for 20 min, washed with tap water, then distilled water, and soaked in distilled water overnight and germinated in a plastic Petri dish with filter paper saturated with distilled water in darkness at 25 °C for 48 h. Lespedeza cuneata [(Dum.-Cours.) G. Don ‘Zhejiang’] seeds were collected from Zhejiang Province, China. Seeds (the seed coat is very soft and does not need sulfuric acid treatment for germination) were soaked in distilled water for 2 h, and then germinated according to the above-described method. After 2 d, seedlings with roots 0·5 cm long were transplanted into a plastic net suspended on a plastic container (2·5 L) filled with 0·5 mM CaCl2 solution (pH 4·5). The solution was renewed every day. After 3 d, uniform seedlings were selected to evaluate Al resistance or to measure the Al content in root tips (0–1·0 cm). The remaining seedlings were transplanted into aerated nutrient solution containing 0 P (–P) or 1·0 mM P (+P) in a 1·5 L container (14 seedlings per pot) and cultivated for 7 d. The nutrient solution was modified from Hoagland solution and consisted of KNO3 (5·0 mM), Ca(NO3)2 (5·0 mMN), MgSO4 (2·0 mM), NH4H2PO4 (1·0 mM), Na-FeEDTA (20 µM), HBO3 (3 µM), MnCl2 (0·5 µM), CuSO4 (0·2 µM), ZnSO4 (0·4 µM) and (NH4)6Mo7O24 (1 µM). NH4Cl (1·0 mM) was substituted for NH4H2PO4 so that the concentration of P was zero. The solution was adjusted to pH 4·5 with 1 M HCl and renewed every 3 d. All the experiments were conducted in an environmentally controlled growth room with a 14 h/25 °C day and 10 h/20 °C night regime, a light intensity of 150 µmol photon m–2 s–1 and a relative humidity of 65 %.
Assessment of Al resistance and determination of Al in the root tips
Al resistance in Lespedeza was examined by measuring the elongation of primary roots of 5-d-old seedlings grown in 0·5 mM CaCl2 solution (pH 4·5) containing 0, 25, 50, 100 or 200 µM AlCl3. Root length was measured with a ruler before and after Al treatment (24 h). Relative root elongation was defined as the percentage of root elongation under Al treatment compared with that of the Al-free control.
The Al content of root tips in samples was determined using a method modified from that of Osawa and Matsumoto (2001). Roots (0–1·0 cm) exposed to various Al concentrations for 24 h were excised and placed in an Eppendorf tube (1·5 mL, ten tips per tube) containing 1 mL of 2 M HCl. The tubes were left to stand for at least 24 h with occasional shaking. Al contents in the solution were determined by inductively coupled plasma-atomic emission spectroscopy (ICP-AES) (IRIS-Advantage, Thermo Elemental, MA, USA) after appropriate dilution.
Alternating Al and P treatment
Intermittent Al treatment was adopted to avoid interactions between Al and other nutrients such as Al–P precipitation. After 1 week in the nutrient solution (–P/ + P), the seedlings were exposed to 0·5 mM CaCl2 (pH 4·5) with or without 50 µM AlCl3 for 1 d and then grown in nutrient solution containing 0 P (–P) or 1·0 mM P (+P) on alternate days. After 30 d of alternating treatment, the Lespedeza seedlings were harvested and separated into shoots and roots.
Morphological analysis of roots
The roots harvested after the alternating experiment were scanned by a root-system scanner, and several parameters including root length, root surface area, root volume, root diameter and the amount of root tips were measured and analysed using the WinRHIZO image analysis system (WIN MAC, Regent Instruments Inc., Quebec, Canada, http://www.regentinstruments.com/).
Mineral contents in plants
After the alternating treatment with Al and P, roots and shoots were dried in an oven for 2 d (70 °C) and ground to a fine powder as necessary. Samples were digested with concentrated HNO3 (heavy-metal grade). Mineral (Al, Ca, Mg, P, K, Mn and Fe) contents were then determined by ICP-AES, after appropriate dilution with 0·1 M HNO3.
Haematoxylin staining test
Haematoxylin is a histochemical indicator used to show the presence of Al. Haematoxylin stain was prepared as described by Polle et al. (1978). It consisted of 0·2 % haematoxylin and 0·02 % KIO3, the dissolution of which was aided by adding a drop of 0·1 M NaOH. Intact seedlings at 4–6 d old were grown in a solution containing 0·5 mM CaCl2 with or without 1·0 mM P at pH 4·5 for 24 h, then treated in 0·5 mM CaCl2 with or without 50 µM Al at pH 4·5 for 3 h. At the end of the treatments, roots were rinsed with distilled water and placed in approx. 60 mL of haematoxylin stain for 40 min with occasional shaking at room temperature. The roots were then placed in the aerated distilled water for 10 min to remove excess stain. The root tips were observed under a light stereoscopic microscope (Olympus-SZX7, Japan) and images were taken with a digital camera. At the same time, Al in the root tips was extracted and determined using the same methods as described above.
Collection of root exudates and determination of organic acids
After 30 d culture in the nutrient solution with or without P as described above, root exudates of the two Lespedeza species were collected. Roots were transplanted to a 0·5 mM CaCl2 solution (pH 4·5) overnight before collection and then exposed to a 0·5 mM CaCl2 solution with or without 50 µM AlCl3 (pH 4·5). After 24 h, root exudates were collected and passed through a cation-exchange column (16 x 14 mm) filled with 5·0 g of Amberlite IR-120B resin (H form), followed by an anion-exchange column (16 x 14 mm) filled with 2·0 g of AG 1-X8 resin (100–200 mesh, formate form) in a cold room. The organic acids retained on the anion-exchange resin were eluted by 2 M HCl, and the eluate was concentrated to dryness using a rotary evaporator (40 °C). After the residue was redissolved in 1·0 mL of ultrapure water, the concentration of organic acids was analysed by high-performance liquid chromatography (HPLC; LC-10AT VP, Shimadzu, Tokyo, Japan) using a Shim-pack SCR-102H column (8·0 mm i.d. x 30 cm) according to Ma et al. (2002).
Statistical analysis
Tukey's test was applied to test differences among treatments at P < 0·05 using the SPSS 13·0 statistical package.
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RESULTS |
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Effects of Al on root growth and Al content
In a dose–response experiment, root elongation of L. bicolor was inhibited by 52, 75, 87 and 92 % after exposure to 25, 50, 100 and 200 µM Al for 24 h, while that of L. cuneata was inhibited by 78, 89, 93 and 97 %, respectively (Fig. 1A). These results showed that L. bicolor had a higher degree of Al resistance than L. cuneata. The Al content in root tips (0–1·0 cm) was lower in L. bicolor than in L. cuneata at each Al concentration tested (Fig. 1B), which indicated that Al exclusion mechanisms may mainly work in Lespedeza.
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Root morphology and fresh weight under Al and P interaction
The root morphology of the two Lespedeza species was determined following a 30 d alternating treatment with 50 µM Al and P solutions. The root morphologies of the two Lespedeza species were similar under –P and +P treatments in Al-free solution, whereas, after Al treatments, obvious differences were seen between the two Lespedeza species (Fig. 2). The root growth of L. cuneata, especially that of the lateral root, was obviously inhibited by Al treatment compared with that of L. bicolor for both –P and +P treatments.
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The root length, root surface area, root volume and the quantities of root tips in L. cuneata significantly decreased under Al stress, while L. bicolor did not exhibit significant inhibition of root growth due to Al treatment except for a decline in root length and root surface area under the –P condition, which was in accordance with the images in Fig. 2 (Fig. 3). Once P was applied, the root length and root surface area did not decrease for L. bicolor under Al stress while this effect was not evident in L. cuneata. Thus, it seemed that P increased the Al resistance of L. bicolor but not in L. cuneata judging from the root morphological parameters.
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Under –P conditions the shoot mass of Al-resistant species was not influenced by Al stress, while it increased significantly under Al stress after P application. However, for Al-sensitive species, the shoot mass changed little under Al stress whether P was applied or not (Fig. 4A), i.e. the effect of Al and P interaction on shoot mass of L. cuneata was insignificant. Neither Al nor P addition had significant effects on the root mass of the two species (Fig. 4B).
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By calculating from the data of Figs 3 and 4, it could be shown that both the separate negative effects of Al ([(+Al) – (–Al)]/(–Al) x 100) and the separate positive effects of P ([(+P) – (–P)]/(–P) x 100) on root morphological parameters and fresh weight of L. cuneata were more obvious than for L. bicolor (Table 1).
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Al and P contents in plants
The Al content in shoots was much lower than that in roots (Fig. 5). Al contents in the roots of the two species increased after P was suppleid, but the extent of the increase was much greater for L. cuneata than for L. bicolor (Fig. 5).
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P contents in shoots and roots of L. bicolor were significantly higher than those in L. cuneata after P was supplied, either with or without Al (Fig. 5). In the presence of P, the P content in roots of L. cuneata increased with Al exposure, but that in shoots decreased, indicating that P transport was constrained from roots to shoots. However, for the resistant species, although the P contents in roots and shoots were decreased when Al was supplied in the presence of P, the decrease of P in shoots was less than that in L. cuneata.
P application led to the augmentation of the P/Al ratio in roots and shoots of the Al-resistant species, while that of the Al-sensitive species was much smaller (Fig. 6).
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Ca, Mg, K, Mn and Fe contents in plant tissues
In the presence of Al, the contents of Ca and Mn in shoots of L. bicolor were reduced but those of Mg and Fe were not (Table 2). Both under P starvation and when P was supplied, interestingly, although the contents of Ca and Mn in shoots of L. cuneata decreased under Al stress, in roots they increased due to Al (Table 2). This result indicated that the transport of nutrients (especially Ca and Mn) to shoots in L. cuneata was restrained by Al stress. The K content of the two species increased with supply of P whether under Al stress or not.
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Effects of supply of P on Al uptake
To investigate further whether the different responses of the two Lespedeza species to P being supplied are associated with Al uptake, the haematoxylin staining method was used in a short-term experiment. The root tips or medial segment of L. bicolor pre-treated with P was stained much less than that not pre-treated with P, but this was not the case for L. cuneata (Fig. 7A).
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The Al content was much lower with +P + Al than with –P + Al in L. bicolor, but not in L. cuneata (Fig. 7B). In addition, the Al content of root tips was significantly lower in L. bicolor than in L. cuneata (Fig. 7B). This result was consistent with the images in Fig. 7A.
Organic acid exudation affected by supply of P
Roots of L. cuneata did not release any organic acids with or without Al exposure. No organic acid anions were detected in root exudates of L. bicolor without Al treatment. However, both citrate and malate were secreted from roots of L. bicolor under Al stress. The Al-induced exudation of organic acids (citrate and malate) under conditions where P was supplied was less than that under P deficiency (Fig. 8).
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DISCUSSION |
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Responses of Lespedeza to the Al and P interaction
Al interferes with a wide range of physical and cellular processes in plants (Kochian et al., 2005). The major symptom of Al toxicity observed in plants is the inhibition of root growth (Delhaize and Ryan, 1995). This extensive root damage results in limited water and mineral nutrient uptake (Barcelo and Poschenrieder, 2002). Relative root elongation of L. bicolor and L. cuneata was 25 and 11 %, respectively, under 50 µM Al for 24 h (Fig. 1A), and nutrient uptake including P, Ca and Mn was significantly reduced after 30 d of Al–P interactions (Fig. 5; Table 2). Thus 50 µM Al was a relative high stress for the Lespedeza especially for L. cuneata.
Ciamporova (2002) indicated that the architecture of the root system can be modified with long-term Al application. As reported by others (e.g. Foy et al., 1978), the detrimental effects of Al are clearly reflected in root development. In this experiment with alternating Al and P treatments, Al–P interactions were partly exhibited as effects on the growth pattern (root morphology and fresh weight, Table 1). Four of the root morphology parameters (length, surface area, volume and root tip numbers) of L. cuneata were inhibited by Al more seriously than those of L. bicolor (Figs 2 and 3). P application reduced the negative effect of Al on root morphology parameters in L. bicolor which was the embodiment of P alleviation on Al toxicity, while in L. cuneata the alleviative effects of P were not significant (Table 1). Compared with the increase in shoot fresh weight caused by Al in L. bicolor especially after P supply, the effect of Al on the fresh weight of L. cuneata was negative (Fig. 4; Table 1). This result was consistent with growth stimulation with Al application (Osaki et al., 1997; Kidd and Proctor, 2000).
Early reports have established that increasing the P supply could alleviate the toxic effects of Al (Tan and Keltjens, 1990a, b). Zheng et al. (2005) concluded that the immobilization of Al with P present in roots was associated with high Al resistance in buckwheat. Foy et al. (1978) suggested that Al absorbed by root surfaces or that in intercellular free spaces may immobilize the P present in the root tissue or external substrates. The effect of Al on maize growth decreased with increasing P content in roots (Gaume et al., 2001). P addition significantly increased Al tolerance in four soybean genotypes differing in P efficiency (Liao et al., 2006). However, from the analysis of the root parameters, the present study suggested that P application could alleviate Al stress in the Al-resistant Lespedeza species to some extent, but not in the Al-sensitive species (Figs 2 and 3). There are several ways in which P might ameliorate the toxic effect of Al in the resistant species, and the main possibilities are discussed below.
Effects of P on the exudation of organic acids by roots under Al stress
Previous results indicated that secretion of malate and citrate from roots was related to the high Al resistance in L. bicolor, and P deficiency did not induce the exudation of organic acids in the two Lespedeza species (Dong et al., 2008). Further results demonstrated that P application significantly reduced the amount of Al-induced organic acid (citrate and malate) exudation in the Al-resistant species under Al stress (Fig. 8), indicating that the decreased exudation of organic acids due to P application could be due to the amelioration of Al toxicity in the resistant species. This result was in accordance with the suggestion by Gaume et al. (2001) that when P was supplied it led to a decrease in organic acid exudation compared with Al exposure without P being supplied in maize. In addition, Dong et al. (2004) provided evidence for root Al and P interactions in that organic acid exudation was differentially induced by Al toxicity and P deficiency in soybean plants, and specific induction of oxalate and malate with P deficiency and citrate exudation with Al stress. Jemo et al. (2007) concluded that the Al-resistant cowpea was better adapted to acidic Al-toxic and P-deficient soils than Al-sensitive cowpea because both malate and citrate exudations were more enhanced by the combined Al and P deficiency. These findings indicated that the type and amount of organic acid release depended on the plant species and external factors, including P deficiency and/or Al stress.
Possible mechanisms of P alleviation of Al toxicity in L. bicolor
Al toxicity and P deficiency often co-exist in acidic soils, so the Al-resistant species, native to the acidic soil might be responsible for mechanisms by which P is used efficiently and there is simultaneous Al detoxification (Foy et al., 1978). Zheng et al. (2005) proposed that Al-resistant buckwheat species had evolved mechanisms to use P efficiently and for there to be simultaneous Al detoxification in acidic soils. Liao et al. (2006) also provided evidence for root Al and P interactions whereby the taproot growth of two P-efficient genotypic soybeans (more Al tolerant) was less affected by Al toxicity than that of two P-inefficient genotypes. Therefore, plants that perform well in low-P acidic soils should possess root systems that are both Al tolerant and P efficient. The present results showed that Al-resistant species had higher P contents than did Al-sensitive species after P was supplied whether Al was present or not, and in Al-sensitive species the decrease in P in shoots was much greater under Al stress compared with that of Al-resistant species (Fig. 5). Therefore, Al might inhibit P transport from roots to shoots in Al-sensitive species.
On the other hand, when P was supplied this resulted in much greater Al accumulation in roots of Al-sensitive species than in Al-resistant species (Fig. 5), and this result could explain the difference in Al damage to the two species. In addition, it was found that P application to Al-resistant species resulted in the augmentation of the P/Al ratio in the roots and shoots, while the increase of the P/Al ratio in Al-sensitive species was much smaller (Fig. 6), indicating that the Al-resistant species possessed a mechanism for constraining Al uptake and facilitating the entry of P. The higher Al resistance in L. bicolor appeared to be associated with higher P and lower Al accumulation in roots. The finding of reduced Al accumulation in root tips of Al-resistant species when P is supplied (Fig. 7) led to the conclusion that P reduced the Al accumulation in root tips of L. bicolor but not in L. cuneata, indicating that Al-resistant species might have greater ability to exclude Al from root tips after P application.
Why P application had no alleviative effect on the Al toxicity in L. cuneata
Acid soils often present a series of stresses to plants including Al toxicity and P deficiency that commonly occur together. The reasons why some plants grow better in these soils might be due to a combination of mechanisms that help overcome each of these stresses separately, or it might be due to a single mechanism that manages to ameliorate both of them. The present study demonstrated, by analysing the root parameters, that P application could not ameliorate Al stress in the Al-sensitive Lespedeza species (Figs 2–4). However, the positive effects of P on root morphology parameters and fresh weight of shoots and roots were higher for L. cuneata than for L. bicolor (Table 1), i.e. the root growth of L. cuneata had a greater response to P application, which hinted that the potential P ameliorative effects on Al stress in L. cuneata may be greater, though this was not shown under the present experimental conditions. The root growth of L. cuneata was greatly constrained under this Al stress (Figs 1 and 3). It suffered significantly more damage to its root tissues than did the more resistant species L. bicolor. This could be a possible reason why P application did not alleviate the Al toxicity in the Al-sensitive species. In acid soils, the effects of P could only be exerted when Al stress is firstly overcome for the Al-sensitive species.
In conclusion, Al resistance of the resistant species, L. bicolor, increased with application of P but that of the Al-sensitive species L. cuneata did not under this relatively high Al stress. Enhancement of Al resistance with the presence of P in the resistant species might be associated with its more efficient accumulation of P and translocation to the shoot; the greater Al exclusion from root tips after P application was also responsible for the alleviative effects of P, but not with the exudation of organic acids in roots. To clarify further why P enhances Al resistance in Al-resistant Lespedeza but not in Al-sensitive Lespedeza, more studies are needed with a wider range of Al levels.
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ACKNOWLEDGEMENTS |
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This work was financially supported by the National Natural Science Foundation of China (contract nos 30571114 and 40621001) and the Chinese Academy of Sciences Knowledge Innovation Program (KSCX2-YW-N-002).
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