Soil Science Society of America Journal 64:949-955 (2000)
© 2000 Soil Science Society of America
DIVISION S-4-SOIL FERTILITY & PLANT NUTRITION
Mechanism of Calcium and Phosphate Release from Hydroxy-Apatite by Mycorrhizal Hyphae
Ricardo L.Lange Nessa and
Paul L.G. Vlekb
a Institute of Agronomy in the Tropics, Grisebachstr. 6, Goettingen 37077, Germany
b Center for Development Research, Univ. of Bonn, Walter-Flex-Str. 3, Bonn 53113, Germany
p.vlek{at}uni-bonn.de
 |
ABSTRACT
|
|---|
The role of vesicular-arbuscular mycorrhiza (VAM) in facilitating the uptake of sparingly soluble nutrients from the soil has been well documented. Uncertainty remains regarding the mechanism controlling the dissolution of tightly bound P such as in phosphate rock. We studied the differential Ca and P uptake by the external mycelium of VAM in maize (Zea mays L.) grown in an acid tropical soil supplied with hydroxy-apatite (HA). Three experiments were conducted in modified double-pot systems where Ca was adequately provided through a nutrient solution and P in the form of apatite through a compartment only accessible to the hyphae. The results showed that in this system: (i) plant uptake of the apatite P occured only with VAM formation, (ii) the P release from the apatite was accompanied by a stochiometrically equivalent buildup of exchangeable Ca in the hyphal compartment, and (iii) the released apatite P was quantitatively recovered by the maize
. It appears that the hyphae drove the apatite dissolution by mass action through the selective absorption of P, thereby overcoming the counter-ion effect due to the Ca accumulation in the soil.
Abbreviations: HA, hydroxy-apatite • PVC, polyvinyl chloride • VAM, vesicular-arbuscular mycorrhiza
|
INTRODUCTION
|
|---|
THE ROLE OF VESICULAR-ARBUSCULAR MYCORRHIZA (VAM) in the acquisition of nutrients from the soil has been long recognized and well documented (Smith and Read, 1997). Particularly with regard to the more immobile plant nutrients in soil, such as P, Zn, and Cu, the role of VAM is often essential (Bolan, 1991; Marschner and Dell, 1994). Three principal mechanisms have been postulated as being responsible for the effect of VAM: (i) the greater exploitation of the soil volume by the hyphal network, thus reducing the diffusion pathway by extending the active absorption surface and enabling access to sites normally not penetrable by roots (Haymann and Mosse, 1972; George et al., 1992); (ii) the higher affinity of hyphae for phosphate as expressed in the Michaelis–Menten equation by a lower Km-value (Cress et al., 1979) and the ability to absorb P at lower solution concentrations than the roots themselves, as expressed by a lower Cm-value (Faquin et al., 1990); and (iii) changes in the rhizosphere by VAM, such as exudation of acids (Rovira, 1969) or chelates (Duff et al., 1963).
Phosphate rock, a sparingly soluble P source, is considered a suitable source of P for tropical soils (Sanchez et al., 1997), where P is often the growth-limiting element (Ssali et al., 1986). Although the pros and cons of using phosphate rock instead of more soluble P sources are still debated (Mokwunye et al., 1986), it has been well established that without the help of VAM this phosphate rock would be too unreactive to benefit most plants. Thirty years ago, Murdoch et al. (1967) showed that VAM were able to make rock-phosphate P available to plants. What remains uncertain is the mechanism by which they manage to extract this P from the apatite matrix (Allen, 1991). As was most recently reported, the mycorrhizal hyphae appear able to enter mineral structures, thus exploiting nutrients otherwise unavailable (Jongmans et al., 1997). Given this remarkable ability, it is indeed of interest to clarify the process by which this is accomplished.
Each of the mechanisms of enhancing the absorption of sparingly soluble P requires the initial dissolution of the apatite in order to allow any of the subsequent reactions to take place. Based on the principles of chemical equilibria, the dissolution of a mineral such as HA is controlled by the law of mass action on the following equilibrium equation:
 | (1) |
This reaction can be driven to the right by the neutralization of the hydroxyl ion, chelation of Ca, and the dissipation or uptake of Ca and P from the dissolution site. The most common assumption has been that hyphae play their role through the exudation of acids. Khasawneh and Doll (1978) pointed out that any process that will reduce the levels of P or Ca around the dissolving mineral will also stimulate its dissolution. The uptake of the elements by the hyphae would be such a process. In 1971, Deist et al. demonstrated that certain plants were able to drive the dissolution of apatite by an efficient absorption of Ca. Proving which of these ions is preferentially absorbed by the plant is complicated by the different nutrient demands of the plants and the myriad of reactions that P may enter into upon its release. The objective of this study was to assess the differential uptake of P and Ca in an acid soil, under conditions of P deficiency and Ca sufficiency as commonly found in nature, and the resulting effect on the dissolution of HA and P uptake by young maize plants.
|
Materials and methods
|
|---|
Experimental Setup
In order to distinguish between uptake of Ca and P by the hyphae, a special apparatus had to be designed. The apparatus had to fulfill the following criteria. First, the HA should be accessible to the hyphae only. Second, the rootable soil volume should be as small as possible. Third, the soil should be low in P and Ca. Fourth, adequate plant nutrition, particularly of Ca, should be assured. The apparatus was a double-pot arrangement described by Janssen (1990) as shown in Fig. 1
. It comprises a soil compartment made of 70-mm-diam. polyvinyl chloride (PVC) pipe in which the phosphate rock and VAM treatments could be arranged, suspended over a 3-L black container with an aerated nutrient solution in order to eliminate artifacts due to nutrient deficiencies other than P. The PVC pipe was cut into three compartments 50 (K1), 20 (K2), and 20 mm (K3) long. A fine polyester screen (30-µm mesh) was placed between the compartments K1 and K2 and between K2 and K3 in order to prevent transgression of roots across compartment boundaries, but not of root hairs and hyphae. The ends of K1 and K3 were capped with PVC lids. The three compartments were then clamped together with the help of four bolts, so that the connections were watertight. In Exp. 1, the system was constructed with compartments K1 and K2 on both sides of K3, thus doubling the soil–HA volume.
View larger version (43K):
[in this window]
[in a new window]
|
Fig. 1 Double-pot system comprising containers for soil and nutrient solution. The soil container is separated into the root compartment (K3), the root-hair compartment (K2), and the hyphae compartment (K1). Hydroxy-apatite (HA) treatments were imposed by addition of HA to K1
|
|
Two 25-mm holes were drilled into the K3 compartment perpendicular to the axis of the pipe, allowing the transplanting and emergence of the shoot and the roots of the maize plant. The adjacent compartment (K2) merely served as a buffer between K3 and K1, preventing root hairs with a maximum extension of 5 mm, from reaching the larger compartment, K1, containing the soil–HA mixture. In the last of the three experiments, a 3-mm air gap was constructed between K1 and K2 to avoid diffusion or mass flow of P and Ca from K1 into K2 (George et al., 1992).
Procedures and Treatments
Prior to assembly, each compartment was tightly packed with 120 g (K2 and K3) and 300 g (K1), respectively, of the appropriate air-dry soil–fertilizer mixture, after bringing it to 80% of field capacity. The soil used was the Ap horizon of an Arenic Kandiustult taken from a cashew (Anacardium occidentale L.) plantation in the state of Ceará in Brazil. It contained 915 g kg-1 sand , 7 g kg-1 C, and 0.4 g kg-1 N. Available P (Bray-1) was 2.3 mg kg-1 and NH4OAc-exchangeable Ca was 0.7 cmol+ kg-1. The soil pH in water was 5.6. The soil was heat-sterilized at 120°C followed by washing with demineralized water, after which Bray P1 was 3.5 mg kg-1 and exchangeable Ca was 0.6 cmol+ kg-1. The HA, Ca5(PO4)3OH, contained 185 g kg-1 P and 399 g kg-1 Ca. In Exp. 1, we studied the effect of rate of HA application on its dissolution and availability. Hydroxy-apatite was added at levels equivalent to 0, 23, 93, and 371 mg P kg-1 soil in K1. In Exp. 2, the treatments were equivalent to 0 and 232 mg P kg-1 soil, but sampling took place after 2, 6, and 8 wk of plant growth to assess the time it took for the hyphae to reach the HA compartment. In the last experiment, the HA levels were similar to Exp. 2, but harvesting and sampling took place after 8 wk only.
Planting material of corn `EPACE 21', a cultivar commonly used in the state of Ceará, was screened for size (35.7 ± 1.4 g 100 seed-1), surface sterilized for 5 min in 100 g kg-1 NaOCl, washed in distilled water, and germinated on filter paper. Three-day-old seedlings were wrapped in rockwool and grown on a nutrient solution, which was gradually changed from a 1:10 to a 1:2 strength of the solution composition proposed by Steiner (1961) and modified after Jungk and Barber (1974) as given in Table 1
. Transplanting took place with uniform, 10-cm-high seedlings, one per unit. For those treatments that required inoculation with mycorrhizal fungi, the seedlings were dipped in a suspension of maize-root inoculum prior to transplanting. Additionally, 2 g of infected root material were placed in the root hole. The inoculum was produced by growing maize plants in sterilized soil, colonized with a highly effective mycorrhiza-forming fungus (Glomus manihotis Howeler) from Colombia (Toro Trujillo, 1992). The inoculum was checked for purity prior to use. Mycorrhiza-free treatments were treated similarly, except that the maize-root suspension was not infected.
Following transplanting, the planting hole was covered with paraffin film to minimize evaporation. The soil–plant container was placed over the hydroponic solution, allowing the roots to grow into the nutrient solution while avoiding direct contact between the soil and the solution, according to the method of Janssen (1990). The nutrient-solution composition for the different experiments was adjusted to pH 5.5 (± 0.2) with KOH. During the first 2 wk, the nutrient solution was exchanged every second day. The nutrient solution for Exp. 2 was a factor 2.75 stronger in P and Ca than for Exp. 1 and 3 (Table 1). After 2 wk, the solution was changed to be free of P and exchanged twice per week (Exp. 1) or once per week (Exp. 2 and 3). Transpired water was replenished three times per week. The experiments were continued for an 8-wk period. Simultaneously, similarly treated soil was placed in containers in the same greenhouse for incubation without plants and sampled at the time of harvest.
The experiments were conducted in the greenhouse facilities of the Institute of Agronomy in the Tropics, University of Goettingen, Germany. Experiment 1 ran from 8 April until 16 June, Exp. 2 from 31 August until 8 Nov. 1993. Experiment 3 was conducted from 26 September until 4 Dec. 1994. Temperatures were regulated with automatic windows and shading, and varied between a maximum of 30°C during the day and 22°C at night. The mean maximum temperature was 27°C and the mean minimum was 22°C. The highest temperatures were recorded in August of 1993. The relative humidity varied between 30 and 70%. The day length averaged 14 h of normal daylight.
Harvest and Analysis
Plants were harvested after 8 wk of growth in the greenhouse. In Exp. 2, additional pots were included to allow sampling after 2 and 6 wk. Plants were cut at the soil surface and the shoots separated into leaves and stems. The roots were harvested separately for the parts that grew in the nutrient solution and in K3. Roots were separated from the soil by hand after washing and sieving the soil, blotted dry, and weighed. Subsamples were taken and weighed for the determination of mycorrhizal colonization. The remaining roots, stems, and leaves were dried separately at 75°C until constant weight was reached.
Dried plant material was ground in a Culatti mill to <1 mm, digested with a perchloric acid–nitric acid (1:2)–hydrochloric acid (6 M) mixture (Juo, 1981), and analyzed for P by the Vanadate–Molybdate method (Kitson and Mellon, 1944). Calcium was analyzed by atomic-absorption spectroscopy (PU9200X, Philips AAS, Eindhoven, the Netherlands). Maize starch (NIST reference material no. 8432, National Institute of Standards and Technology, Gaithersburg, MD) served as an analytical reference. The extent of VAM development was determined following staining of the preserved root material by a modified trypan-blue-glycerin method (Koske and Gemma, 1989), using the line intersection method of Giovannetti and Mosse (1980).
Plant-available P in soil was extracted by the mildly alkaline Olsen method (Watanabe and Olsen, 1965) in order to avoid the aggressive dissolution of the apatite, which would be expected with the common acid extraction methods. Exchangeable Ca was determined with the BaCl2 method of Bascomb (1964), described by Kanabo and Gilkes (1987), thus eliminating dissolution from HA.
All experiments were conducted in a completely randomized design with rerandomization at each change of nutrient solution in order to eliminate border effects. Experiment 1 included three replications and Exp. 2 had four replications, whereas in the third experiment the number of replications varied between two and eight because of the early demise of some plants. All data of Exp. 1 and 2 were subjected to a two- or three-factorial analysis of variance. Significant differences in treatment effects were established using the Tukey test
or, in the unbalanced Exp. 3, by calculating the standard error of the means.
|
Results and discussion
|
|---|
Phosphorus Uptake
Mycorrhizal development in maize was significantly increased by the application of HA at any rate to the soil in K1, changing from 30% in the absence of HA to between 60 and 70% with HA in Exp. 1. These differences were 40 vs. 60% in Exp. 2 and 30 vs. 50% in Exp. 3. The rate of HA application in Exp. 1 did not have a significant effect on the VAM formation. Results from Exp. 2 showed that the effect of HA on VAM was not noticeable after the first 2 wk when the proportion of roots showing mycorrhizal structures was only 35% irrespective of HA presence. After 6 wk, the differences were significant
and had reached the levels given above. Without inoculation, no mycchoriza development was discernable.
Phosphate uptake by the maize plants reflected the access of the plant to apatite P. The VAM formation combined with the addition of HA to the outer compartment (K1) significantly increased P uptake by maize. However, in Exp. 1 and 3, the addition of HA or VAM alone was not enough to significantly increase the P uptake by maize (Table 2)
. Experiment 1 further revealed that, even with VAM, only the two highest levels of HA resulted in significantly increased P uptake, from 25 to 34 and 46 mg P plant-1, respectively.
View this table:
[in this window]
[in a new window]
|
Table 2 Dry matter production and phosphate uptake after 8 wk of maize growth as affected by vesicular-arbuscular mycorrhiza (VAM) infection and hydroxy-apatite (HA) application to the outer compartment (K1) for the three experiments
|
|
The effect of VAM on P uptake in Exp. 2 is not evident from Table 2. In this experiment, a change to a higher concentrations of P and Ca in the nutrient solution was considered necessary to compensate for the reduction in soil volume as compared with Exp. 1. However, the ample P supply led to more vigorous growth (Table 2) and luxury consumption of P by the maize plants during the first 2 wk of P uptake. The accumulated P largely sufficed for plant growth during the following 6 wk of rapid growth (11 g wk-1). Additional P appears to have been accessed by the VAM from the HA, as reflected in the significantly increased P uptake in this treatment at 6 wk (Fig. 2)
. The effect of fungal inoculation is first reflected in P uptake after 6 wk of growth, consistent with the time it took to show differences in VAM development in this experiment. Growth between 6 and 8 wk slowed down to 3 g wk-1 and appeared to cause stress in all treatments, most likely due to root binding. This led to a decrease in the total plant P in all treatments, particularly in those without HA. The results of Exp. 2 led to a reversion to the lower-strength nutrient solution in Exp. 3.
View larger version (16K):
[in this window]
[in a new window]
|
Fig. 2 Phosphorus uptake by maize with vesicular-arbuscular mycorrhiza (VAM) after 2, 6, and 8 wk of growth on soil with and without hydroxy-apatite (HA) in Exp. 2, showing significantly increased P uptake for the HA- and VAM-treated plants than for the other treatment after 6 wk of growth. Honestly significant difference (0.05) after Tukey
|
|
Delta-Calcium
The effect of mycorrhiza on the chemical dynamics of HA in the outer chamber (K1) was assessed by tracing the concentration of exchangeable Ca and Olsen P in that chamber at final harvest (Table 3)
. Without VAM in Exp. 1, Ca levels of K1 for the HA-treated soil on which maize was grown were similar to those for the incubated soil, indicating that Ca was not taken up or did not move out of K1. However, Ca levels in K1 were significantly increased by the inclusion of VAM into the soil–plant system. Combined with the significant reduction in Olsen-P due to VAM, this is an indication that P was selectively absorbed by the hyphae. This pattern was repeated in Exp. 2 and 3. However, a significant reduction in exchangeable Ca was noted in the absence of VAM as compared with the incubated soil of Exp. 2 and to a lesser extent in Exp. 3 without the air gap, suggesting that some Ca movement to compartment K2 had occurred. This was confirmed in Exp. 2 by a significant increase in K2 from 123 to 138 mg Ca kg-1, irrespective of VAM development. The greater movement of Ca in Exp. 2 may have been related to the greater biomass production in this experiment providing a strong sink for soil nutrients (Table 2). The Ca levels in the neighboring compartment (K2) in Exp. 3 showed a significant enrichment in Ca to 181 ± 4.5 mg kg-1 when no air gap was present. The Ca levels in K1 and K2 in Exp. 3 were not significantly different from those of the incubated soil in the presence of an air gap. Irrespective of the air gap, an enrichment of Ca in K1 took place when VAM was present (i.e., from 230 to 
273 mg kg-1) consistent with findings from Exp. 1 and 2. Thus, VAM caused an increase in exchangeable Ca of between 7% (Exp. 1) and 20% (Exp. 3 with air gap), making it unlikely that the hyphae used Ca uptake as a means of gaining access to HA P.
View this table:
[in this window]
[in a new window]
|
Table 3 Exchangeable Ca and Olsen extractable P in the 8-wk incubated soil and in the outer compartment (K1) and 8 wk of plant growth
|
|
The exchangeable Ca in the outer chamber derived from the applied HA is calculated as the difference between the native exchangeable Ca in the unamended soil following an 8-wk incubation (122, 123, and 151 mg Ca kg-1 for experiments 1, 2, and 3, respectively), and that found at harvest in the soil of K1 after application of HA (Table 3). This value, which assumes that all of the dissolved Ca ends up in an exchangeable form, is commonly referred to as delta-Ca (Kanabo and Gilkes, 1987). The equivalent parameter for P (delta-P) cannot be obtained in a similar way, as the redistribution of dissolved P in the soil may render a good fraction of it in insoluble forms such as strengite or variscite. Given stochiometric dissolution of Ca5(PO4)3OH, we may calculate a derived delta-P as the proportional amount of P to have been codissolved with the Ca. Therefore, the actual amounts of HA P dissolved may be best surmised from the delta-Ca values, assuming stochiometric dissolution and a Ca/P mass ratio of 2.16 in HA.
In Exp. 1, the delta-Ca values of K1 when VAM was absent were essentially the same as those of the incubated soil with the same rate of HA applied, indicating that little or no Ca had been extracted or moved by the plant from the outer chamber. In Exp. 2, Ca depletion of K1 was observed in the noninoculated treatment, which resulted in significantly lower delta-Ca value (28 mg Ca kg-1) after 8 wk of plant growth than in the soil incubated for the same period (50 mg Ca kg-1). In Exp. 3, it was confirmed that some Ca was able to move from K1 to K2 when no air gap was present, enough to cause a significant increase from 159 ± 5.0 to 181 ± 2.6 mg Ca kg-1 in K2 as well as in the larger compartment, K1 (Table 3). As a result, estimating the dissolved fraction of applied HA in K1 from delta-Ca may lead to an underestimation because of loss of Ca from the compartment. In Exp. 3, the inclusion of an air gap between K1 and K2 effectively eliminated Ca transfer between chambers.
After inoculation with G. manihot, the delta-Ca values of K1 increased significantly in all experiments. In Exp. 1, the values for the different application rates of HA increased from 12 to 20, 28 to 39, and 65 to 79 mg Ca kg-1, due to additional dissolution of Ca from HA due to VAM (Table 4)
. Assuming stochiometric dissolution of HA, having a Ca/P mass ratio of 2.16, this should have released an additional 3.7, 5.1, and 6.5 mg P kg-1, or an average of 5.1 mg P kg-1, as a result of VAM formation. In Exp. 2, where a single rate of HA was applied, the delta-Ca had not changed from that of the incubated soil after 2 wk of plant growth (54 vs. 50 mg Ca kg-1). Once the hyphae reached the K1 chamber (6 wk), the delta-Ca increased significantly to 67 mg Ca kg-1, while the delta-Ca in the incubated soil remained constant at 50 mg Ca kg-1. After 8 wk, the delta-Ca had increased to 78 , indicating a continued dissolution of HA which, during the 8-wk period, should have made available an additional 13 mg P kg-1. In Exp. 3, the estimated delta-P increase was 18 mg P kg-1 without the air gap, and 22 mg P kg-1 with an air gap, leading to an underestimation of up to 22% if no air gap was present. Using the VAM-free treatment as a reference rather than the incubated soil corrects for this underestimation and yields a delta-P increase of 22 mg P kg-1 as well.
View this table:
[in this window]
[in a new window]
|
Table 4 Delta-Ca for the 8-wk incubated soil (Inc) and the soil of the outer chamber (K1) after 8 wk of plant growth with vesicular-arbuscular mycorrhiza (VAM) and the delta-P derived thereof, representing the dissolved hydroxy-apatite (HA) and the corresponding P taken up by maize
|
|
If the dissolution of the phosphate rock was driven by the P demand of the maize, we might expect to recover the dissolved P in the plant biomass. The P uptake by the plants is reported in Table 2 on the basis of the amount of soil in K1, which was 600 g for Exp. 1 or 300 g for Exp. 2 and 3. The additional P uptake due to HA in the VAM systems was estimated by subtracting the HA-free values from the HA-treated values. On average for the three application rates in Exp. 1, the extra P uptake was 12.1 mg kg-1, which corresponds with 13.6 mg kg-1 P that was supposedly available (delta-P in K1 at harvest). In Exp. 2 and 3, the extra P uptake was 8.8, 16.4, and 12.9 mg pot-1, respectively, which corresponds with the delta-P, expressed on a 300 g of soil basis, of 10.8, 16.4, and 17.5 mg P. Given the complexity of the system this may be considered a good agreement (Table 4).
Olsen Phosphorus
Given the fact that the maize plants recovered most of the liberated P as assessed by the delta-P values in K1, none of the initially available P should be left in these compartments after harvest. However, the extractions of the HA-amended K1 soil with Olsen solution after harvest were not negligible, indicating remaining available P. Presumably, this P could be dissolved from the rock during extraction. However, experiments with double and triple extraction with Olsen solution revealed that no additional P could be extracted following the first extraction, even if the HA was left to interact with the moist soil following the first extraction with Olsen solution. Thus, it appears that the hyphae derive their P, at least in part, from a different fraction of the HA minerals than the Olsen extract dissolves. This is illustrated in Table 3, showing that up to 23 mg P kg-1 of HA were still extractable from the soil–HA mixture during Olsen extraction following harvesting. Thus, the Olsen P method cannot be used to quantify the residual available P or predict the uptake of P by plants from the soil–HA mixture.
|
Conclusions
|
|---|
The principle objective of this study was to verify whether mycorrhizal plants were dependent on the uptake of the counter ion of phosphate in HA, Ca, in order to gain access to the P, as postulated by Deist et al. (1971) and Bolan (1991). The results of the three experiments provided evidence that this is not necessarily the case. In our experimental setup it was made certain that Ca was adequately supplied through a double-pot technique in which Ca was available in the nutrient solution throughout the growing period of 8 wk. This is a situation often found in P-limiting soils. Under these conditions, we have shown that, as soon as the supply of P in the nutrient solution was interrupted, the maize plants became dependent on their mycorrhizal symbiosis for access to the P in the HA supplied to the outer chamber. The exception was Exp. 2, where the much larger biomass accumulation appears to have exerted a great demand pressure on the soil even without the help of VAM. In Exp. 1 and 3, where dry matter accumulation was only about one-third of that in Exp. 1, the HA in the outer chamber was not taken up by the plants if no mycorrhiza was introduced into the system.
The addition of HA to the soil led to the dissolution of a fraction of the HA, most likely due to the inherent acidity of the soil (Mokwunye et al., 1986). This fraction was estimated by the increase in exchangeable Ca (delta-Ca) resulting from the dissolution, from which the HA-derived P could be calculated (delta-P). It is commonly assumed that no direct way of estimating delta-P can be devised due to the complexity of the reactions that the released P enters.
The activity of the hyphae in the outer chamber led to a significant further release of Ca from the HA as expressed by an increase in delta-Ca. The mechanism involved appears to confirm the process postulated by Haymann and Mosse (1972) in which the close contact between hyphae and the HA surface where dissociation takes place plays an important role. Indeed, with greater additions of HA, larger amounts of Ca were set free and accumulated in the outer chamber.
The accumulation of Ca due to hyphal activity and the concomitant reduction in extractable Olsen P disprove the hypothesis that the extraction of the counter ion from the HA by the hyphae was the driving force for the dissolution process as suggested by Bolan (1991). In fact, to continuously dissolve HA as was demonstrated in Exp. 2, the dissolution had to take place despite a reduced gradient as the equilibrium P concentration at the dissolution site would be depressed as a result of mass action by the buildup of Ca (Eq. [1]). Numerous mechanisms for this phenomenon have been suggested, such as the development of siderophores (Jayanchandran et al., 1989), the exudation of organic acids (Rovira, 1969) that may either change the solubility of HA due to the reduction in pH (Moghimi and Tate, 1978), or due to their chelating effect (Duff et al., 1963). Our studies did not elucidate the mechanism involved.
|
ACKNOWLEDGMENTS
|
|---|
The support of the German Academic Exchange Program (DAAD) and the Brazilien National Research Center Fellowship Program (CNPq) to the senior author are gratefully acknowledged.
Received for publication April 6, 1999.
|
REFERENCES
|
|---|
- Allen M.F. The ecology of Mycorrhizae. Cambridge, UK: Cambridge Univ. Press, 1991.
- Bascomb C.L. Rapid method for determination of cation-exchange capacity of calcareous and non-calcareous soils. Sci. Food Agric. 1964;15:821-823.
- Bolan N.S. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 1991;134:189-207.
- Cress W.A., Throneberry G.O., Lindsey D.L. Kinetics of phosphorus absorption by mycorrhizal and non-mycorrhizal tomato roots. Plant Physiol. 1979;64:484-487.[Abstract/Free Full Text]
- Deist J., Marais P.G., Harry R.B., Heyns C.F.-G. Relative availability of rock phosphate to different plant species. Agrochemophysica 1971;3:35-40.
- Duff R.B., Wembley D.M., Scott R.O. Solubilization of minerals and related materials by 2-ketogluconic acid producing bacteria. Soil Sci. 1963;95:105-114.
- Faquin V., Malavolta E., Muraoka T. Cinética da absorçao de fosfato em soja sob influência de micorriza vesícolo-arbuscular. Revista Basiliensa di Ciensia do Solo 1990;14:41-48.
- George E., Häussler K.U., Vetterlein D., Gorgus E., Marschner H. Water and nutrient translocation by hyphae of Glomus mosseae. Can J. Bot. 1992;70:2130-2137.
- Giovannetti M., Mosse B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 1980;84:489-500.
- Haymann D.S., Mosse B. Plant growth responses to vesicular-arbuscular mycorrhiza. III. Increased uptake of labile P from soil. New Phytol. 1972;71:41-47.
- Janssen, B.H. 1990. A double-pot technique as a tool in plant nutrition studies p. 759–763. In M.L van Beusinchem (ed.) Plant nutrition—Physiology and applications. Kluwer Academic Publ., Dordrecht, the Netherlands.
- Jayanchandran K., Schwab A.P., Hetrick B.A.D. VA Mycorrhizal mediation of phosphorus availability: Synthetic iron chelate effects on phosphorus solubilization. Soil Sci. Soc. Am. J. 1989;53:1701-1706.[Abstract/Free Full Text]
- Jongmans A.G., van Breemen N., Lundström U., van Hees P.A.W., Finlay R.D., Srinivasan M., Unestam T., Giesler R., Melkerud P.-A., Olsson M. Rock-eating fungi. Nature (London) 1997;389:682-683.
- Jungk A., Barber S.A. Phosphate uptake rate of corn roots as related to the proportion of the roots exposed to phosphate. Agron. J. 1974;66:554-557.[Abstract/Free Full Text]
- Juo A.S.R. Automated and semi-automated methods for soil and plant analysis. Manual Series no. 7. Ibadan, Nigeria: IITA, 1981.
- Kanabo I.A.K., Gilkes R.J. The influence of the addition of goethite to soil on the dissolution of North Carolina phosphate rock. Aust. J. Soil Res. 1987;25:313-322.
- Khasawneh F.E., Doll E.C. The use of phosphate rock for direct application to soils. Adv. Agron. 1978;30:159-206.
- Kitson R.E., Mellon M.G. Colorimetric determination of phosphorus as molybdivanando phosphoric acid. Ind. Eng. Chem. Anal. Ed. 1944;16:379-383.
- Koske R.E., Gemma J.N. A modified procedure for staining of roots to detect VA mycorrhizas. Mycol. Res. 1989;92:486-505.[ISI]
- Marschner H., Dell B. Nutrient uptake in mycorrhizal symbiosis. Plant Soil 1994;159:89-102.
- Moghimi A., Tate M.E. Does 2-ketogluconate chelate calcium in the pH range 2.4 to 6.4?. Soil Biol. Biochem. 1978;10:289-292.
- Mokwunye A.U., Chien S.H., Rhodes E.R. Reactions of phosphate with tropical African soils. In: Mokwunye A.U., Vlek P.L.G., eds. Management of nitrogen and phosphorus fertilizers in sub-Saharan Africa. Dordrecht, the Netherlands: Martinus Nijhoff Publ, 1986:283-318.
- Murdoch C.L., Jacobs J.A., Gerdemann J.W. Utilization of phosphorus sources of different avialability by mycorrhizal and non-mycorrhizal maize. Plant Soil 1967;27:329-334.
- Rovira A.D. Plant root exudates. Bot. Rev. 1969;35:35-57.
- Sanchez P.A., Shephard K.D., Soule M.J., Place F.M., Buresh R.J., Izac A.-M.N., Mokwunye A.U., Kwesiga F.R., Nditiru C.G., Woomer P.L. Soil fertility replenishment in Africa: An investment in natural resource capital. In: Buresh R.J., et al. , ed. Replenishing soil fertility in Africa. Madison, WI: SSSA and ASA, 1997:1-46 SSSA Spec. Publ. 51..
- Smith S.E., Read D.J. Mycorrhizal symbiosis. London, UK: Academic Press, 1997.
- Steiner A.A. A universal method for preparing nutrient solution of a certain desired composition. Plant Soil 1961;2:134-154.
- Ssali H., Ahn P., Mokwunye A.U. Fertility of soils of tropical Africa: A historical perspective. In: Mokwunye A.U., Vlek P.L.G., eds. Management of nitrogen and phosphorus fertilizers in sub-Saharan Africa. Dordrecht, the Netherlands: Martinus Nijhoff Publ, 1986:59-82.
- Toro Trujillo S. Wechselbeziehungen in der Rhizosphäre zwischen floureszierenden Pseudomonaden und vesikulärarbus-kulären Mykorrhizzapilzen und ihre Auswirkung auf das Wachstum von Sorghum bicolor (L.) Moench. Goettingen, Germany: Goettinger Beiträge zur Landund Forstwirtschaft in den Tropen und Subtropen Verl Erich Goltze, 1992.
- Watanabe F.S., Olsen S.R. Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extract from soil. Soil Sci. Soc. Am. Proc. 1965;29:677-678.
TOP
ABSTRACT
INTRODUCTION
