AOBPreview originally published online on June 28, 2004
Annals of Botany 2004 94(2):297-303; doi:10.1093/aob/mch140
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Annals of Botany 94/2, © Annals of Botany Company 2004; all rights reserved
Acid Phosphatase Role in Chickpea/Maize Intercropping
1 Department of Plant Nutrition, China Agricultural University, Beijing, 100094, China, 2 Resource and Environmental College, Northeast Agricultural University, Harbin, 150030, China and 3 Department of Agricultural Sciences, La Trobe University, Bundoora, Vic. 3086, Australia
* For correspondence. E-mail lilong{at}cau.edu.cn
Received: 8 September 2003 Returned for revision: 9 February 2004 Accepted: 19 April 2004 Published electronically: 28 June 2004
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and aims Organic P comprises 30–80 % of the total P in most agricultural soils. It has been proven that chickpea facilitates P uptake from an organic P source by intercropped wheat. In this study, acid phosphatase excreted from chickpea roots is quantified and the contribution of acid phosphatase to the facilitation of P uptake by intercropped maize receiving phytate is examined.
• Methods For the first experiment using hydroponics, maize (Zea mays ‘Zhongdan No. 2’) and chickpea (Cicer arietinum ‘Sona’) were grown in either the same or separate containers, and P was supplied as phytate, KH2PO4 at 0·25 mmol P L–1, or not at all. The second experiment involved soil culture with three types of root separation between the two species: (1) plastic sheet, (2) nylon mesh, and (3) no barrier. Maize plants were grown in one compartment and chickpea in the other. Phosphorus was supplied as phytate, Ca(H2PO4)2 at 50 mg P kg–1, or no P added.
• Key results In the hydroponics study, the total P uptake by intercropped maize supplied with phytate was 2·1-fold greater than when it was grown as a monoculture. In the soil experiment, when supplied with phytate, total P uptake by maize with mesh barrier and without root barrier was 2·2 and 1·5 times, respectively, as much as that with solid barrier. In both experiments, roots of both maize and chickpea supplied with phytate and no P secreted more acid phosphatase than those with KH2PO4 or Ca(H2PO4)2. However, average acid phosphatase activity of chickpea roots supplied with phytate was 2–3-fold as much as maize. Soil acid phosphatase activity in the rhizosphere of chickpea was also significantly higher than maize regardless of P sources.
• Conclusions Chickpea can mobilize organic P in both hydroponic and soil cultures, leading to an interspecific facilitation in utilization of organic P in maize/chickpea intercropping.
Key words: Intercropping, acid phosphatase, Cicer arietinum, phosphorus, chickpea, root barrier, facilitation, monoculture, phytate, Zea mays
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Intercropping is becoming more and more important to increase crop productivity to meet food demands of an increasing population, especially in the northwest China (Li et al., 1999
). Intercropping, through effective use of water, nutrients and solar energy, can significantly enhance crop yields compared with monoculture cropping (Willey, 1990; Morris and Garrity, 1993). When two crops are planted together, interspecific competition or facilitation between plants may occur (Vandermeer, 1989). For example, mixtures of cereals and lupins produced higher grain yields than either crop grown alone; the yield increases were not only due to an improved nitrogen nutrition of the cereal component, but also to other unknown causes (Nel, 1975). Maize yield was increased by intercropping with groundnut, mainly because of an enhanced P uptake (El Dessougi et al., 2003). White lupin (Lupinus albus) exuded organic acids to mobilize sparingly soluble phosphate which made more P available for wheat than when it was grown as a monoculture (Horst and Waschkies, 1987; Kamh et al., 1999). Pigeon pea increased P uptake of the intercropped sorghum by exuding piscidic acid that chelates Fe3+ and subsequently releases P from FePO4 (Ae et al., 1990). In a field experiment, faba bean facilitated P uptake by maize (Li et al., 2003b). However, all these studies were focused on inorganic P in the soil.
In most agricultural soils, organic P comprises 30–80 % of the total P (Dalal, 1978). The largest fraction of organic P, approx. 50 %, is in the form of phytin and its derivatives (Tarafdar and Claassen, 1988). Organic P sources can be utilized by the plant after they are hydrolysed by phosphatase (Gilbert and Knight, 1999). Agroforestry species with high acid phosphatase activities can mobilize and utilize organic P in the soil (George et al., 2002a). Chickpea could facilitate P uptake by associated wheat from an organic P source (Li et al., 2003a). The mechanism involved, however, remains unclear. The objectives of this study were to quantify acid phosphatase excreted from chickpea roots and to examine whether acid phosphatase contributed to the facilitation of P uptake of intercropped maize that had been supplied with phytate.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Plant materials and growth conditions
Experiment 1
The first experiment, with four replicates, was conducted with hydroponics culture in a growth chamber at 25–27 °C day/18–20 °C night with 14 h photoperiod (250 µmol m–2 s–1). It consisted of three P and three planting treatments. The three P treatments were (1) without P addition (P0), (2) 0·25 mmol L–1 P as KH2PO4, and (3) 0·25 mmol L–1 P as phytate-Na (C6H6O24P6Na12, SIGMA P-3168). The three planting treatments were (1) four plants of maize (Zea mays L. ‘Zhongdan No. 2’) as a monoculture, (2) eight plants of chickpea (Cicer arietinum L. ‘Sona’) as a monoculture, and (3) two plants of maize and four plants of chickpea as a mixed culture.
Seeds of chickpea and maize were surface-sterilized in 5 % H2O2 for 30 min, pregerminated in the dark in a Petri dish with adequate water, and were then planted in quartz sand. After 7–8 d, plants were transplanted to 2 L containers with half-strength nutrient solution for the first 3 d, and thereafter grown in full- strength nutrient solution with or without a P supply. The nutrient solution consisted of K2SO4 0·75 x 10–3, MgSO4 0·65 x 10–3, KCl 0·1 x 10–3, Ca(NO3)2 2·0 x 10–3, H3BO4 1·0 x 10–7, MnSO4 1·0 x 10–3, CuSO4 1·0 x 10–7, ZnSO4 1·0 x 10–6, (NH4)6MO4O24 5·0 x 10–9 and EDTA-Fe 1·0 x 10–4 mol L–1. KCl (0·25 mM L–1) was added to the phytate and no P treatments to equalize the amount of potassium in the KH2PO4 treatment. The pH of the nutrient solution was adjusted to 6·0 and the solution was renewed every 3 d. During the whole experiment, the containers were continuously aerated.
Experiment 2
The experiment consisted of three P treatments and three treatments of root separation between maize and chickpea. The three P treatments were (1) no added P, (2) Ca(H2PO4)2·H2O (orth-P), 50 mg P kg–1 soil (calcium salt was used to avoid adding extra potassium to the soil), and (3) phytate-Na, 50 mg P kg–1 soil. Three root separations were (1) plastic sheet to eliminate root contact and solute movement, (2) nylon mesh (30 µm) to prevent root contact but permit solute exchange, and (3) no root separation (Fig. 1). Plastic pots (0·15 m diameter) were cut in the middle, separated into two compartments and then re-constructed.
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Each compartment of the pot was filled with 1·5 kg of air-dried and sieved (2 mm) soil. The soil was a low P sandy soil collected from Lu Gouqiao Bridge in the northeast of Beijing. The soil contained 4·2 g organic matter, 0·3 g total N, 1·7 mg NaHCO3-extractable P and 48·9 mg K per kg soil, and had a pH (extracted by solution of 0·01 mol L–1CaCl2, with soil : solution of 1 : 5) of 7·8. Basal nutrients (without P) were added in solution to soil (mg kg–1 soil): N 200 mg as NH4NO3, K 200 mg as KNO3, Mg 50 mg as MgSO4·7H2O, Fe 5 mg as FeSO4·7H2O, Mn 5 mg as MnSO4, Cu 5 mg as CuSO4·5H2O and Zn 5 mg as ZnSO4·7H2O. The soil was thoroughly mixed by shaking. Six germinated seeds of chickpea and four seeds of maize were grown in the pot (one species in each compartment). Plants were thinned to five per compartment for chickpea and to two for maize 10 d after sowing. The pots were watered daily to field capacity (16 %, w/w).
Harvesting and soil sampling
Experiment 1
After transplanting for 15 d in nutrient solution, one plant of maize and two plants of chickpea were sampled from each container every 5 d. Plant roots were thoroughly washed with distilled water for assay of acid phosphatase activity. Dry weights of roots and shoots were recorded. Phosphorus concentration in plant tissues was determined using the vanodomolybdate method (Westerman, 1990) after the plant material was digested in concentrated H2SO4.
Experiment 2
The plants were harvested 40 d after sowing. Roots were separated from soil; any soil remaining on the surfaces of roots was brushed off and the soils placed immediately in a cold room at 4 °C. Dry weights and P concentrations in shoots were measured with the same methods as in expt 1.
Phosphatase activity
In expt 1, the phosphatase activity of intact roots was assayed using the method of Mclachlan (1980). Roots were washed in distilled water, blotted dry and then immersed in 0·1 mol L–1 acetate buffer (pH 5·6) containing p-nitrophenyl phosphate at 30 °C for 1 h. Blanks containing all ingredients except the living material were included under the same conditions and sampled at the same time as the assay. In expt 2, the activity of acid phosphatase in soil was analysed within 7 d after sampling by the method of Tarafdar and Jungk (1987) using acetate buffer (0·1 mol L–1, pH 5·6) and p-nitrophenyl phosphate as a substrate at 30 °C for 1 h. One unit of acid phosphatase activity was the amount of enzyme per gram root fresh weight or per g soil which produced 1 µmol of p-nitrophenyl per hour.
Root length
Viable roots of plants were spread without overlaps onto a glass plate. The root length was measured by a leaf area scanner (CI-203 area meter, CID Corporation Ltd, USA).
Statistical analysis
The experiments were set up in a completely randomized design. Statistical significance of differences between treatments was analysed by analysis of variance (ANOVA) and LSD (least significant difference) multiple comparison (SAS Institute, 1985).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Biomass
In expt 1, the total biomass of maize (combining intercropping and sole) supplied with KH2PO4 was significantly greater than that with phytate, which was greater than the control (without P), indicating that the P supply from phytate was inadequate for optimal plant growth (Fig. 2). When the plants were intercropped with chickpea and supplied with phytate, the maize biomass was increased almost 2-fold as compared with monoculture supplied with phytate. However, when plants were supplied with KH2PO4 or no P was supplied, no significant difference in biomass was observed between monoculture and intercropped maize. Average chickpea biomass of intercropped and monoculture was similar when P was received as KH2PO4 or phytate but was greater than that without P (Fig. 2). The cropping system did not affect chickpea biomass regardless of P source.
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In expt 2, the greatest biomass of maize was observed in the Ca(H2PO4)2 treatment, and was significantly greater than that of plants supplied with organic P (phytate) or without P addition (Fig. 3). When plants were intercropped with chickpea and supplied with phytate, the biomass of maize without root separation and with nylon mesh was increased by 49 % and 75 %, respectively, as compared with that with the solid barrier (Fig. 3). When P was supplied by Ca(H2PO4)2, the biomass of maize was highest with no root barrier; this was significantly higher than the biomass of the maize with the solid barrier (Fig. 3). This effect was proportionally more striking when P was supplied as phytate (Fig. 3). For chickpea, the biomass of plants separated from the maize by nylon mesh or plastic sheet was significantly higher than that without the barrier when P was supplied as either Ca(H2PO4)2 or phytate (Fig. 3).
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The combined biomass of maize and chickpea without root barrier (3·30 g pot–1) or with nylon mesh barrier (4·04 g pot–1) supplied with phytate was greater than those with the solid barrier (2·75 g pot–1), indicating that yield advantages of maize intercropped by chickpea were due to interspecific root interactions.
Phosphorus
In expt 1, the P concentration in maize shoots was highest in the treatment of KH2PO4, followed by the phytate treatment, and lowest in the no P control. Phosphorus concentration in shoots of the intercropped maize supplied with phytate was 12 % higher than that of the monoculture (Fig. 4). However, intercropping did not significantly affect P concentration in maize shoots in the other two P treatments. In comparison, in chickpea no significant difference was observed in the average P concentration of monoculture and intercropped plants supplied with phytate versus KH2PO4 (Fig. 4). Total P uptake by intercropped maize supplied with phytate was 2·1-fold higher than in monoculture; however, a compensating decrease in total P uptake by chickpea did not occur (Fig. 5). There was no significant difference in total P uptake by intercropped maize and monoculture one when no P was added or when P was supplied by KH2PO4 (Fig. 5).
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In expt 2, when phytate was supplied, P concentration in maize shoots was 28 % greater with nylon mesh barrier than that with solid barrier (Table 1). P concentrations in shoots of maize supplied with Ca(H2PO4)2 without root barrier and with mesh barrier were 38 % and 19 % higher than that with solid barrier, respectively. When supplied with phytate or Ca(H2PO4), total P uptake by maize with no barrier or mesh barrier was significantly higher than with solid barrier.
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In contrast to maize, when chickpea plants were supplied with phytate, P concentration with solid barrier and with mesh barrier was significantly greater than that without root barrier (Table 1). Chickpea with solid barrier had the most P uptake among the treatments of root separation regardless of P sources.
Total P uptake by maize and chickpea with mesh barrier was greater than that with solid barrier indicating that P uptake was facilitated by intercropping.
Acid phosphatase activity
In expt 1, acid phosphatase activity of plant roots supplied with organic P or without P was significantly enhanced compared with those grown in inorganic P. Average acid phosphatase activity of intercropped and monoculture maize supplied with phytate or no P addition was 81 % and 62 % greater than that supplied with KH2PO4 at Day 20, respectively (Fig. 6). Average acid phosphatase activity secreted from intercropped and monoculture chickpea roots supplied with phytate was 3·0-fold greater than maize at Day 20 (Fig. 6). Similar results for maize and chickpea were observed at Day 15 and Day 25, respectively. Compared with maize, the magnitude of increase in acid phosphatase activity of chickpea was less than that of maize at Day 15 but was greater than that of maize at later days (data was not shown).
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In expt 2, soil acid phosphatase activity in the rhizosphere had a similar trend to that of plant roots in the hydroponic culture (expt 1) but, the magnitude of increase was much lower than that in expt 1. Average soil acid phosphatase activity (combining the data from all root barrier treatments) in the rhizosphere of chickpea roots (1·5 µmol g–1 h–1) supplied with phytate was twice as high as that of maize (0·74 µmol g–1 h–1; Fig. 7).
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Root length
Average root length of maize without P addition was increased by 24 % compared with KH2PO4 treatment (combined data from monoculture and intercropped; Fig. 8). The root length of intercropped maize was significantly increased compared with monoculture regardless of P source. No significant difference was observed in the root length of chickpea between P sources. The intercropping also does not significantly affect the root length of chickpea.
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DISCUSSION |
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Maize growth increases result from the improvement of phosphorus nutrition
The present study demonstrated that intercropping of maize and chickpea facilitated the growth of maize when P was supplied as phytate, an organic form (Figs 2 and 3). This is consistent with the findings of Li et al. (2003a)
that chickpea facilitated the growth of intercropped wheat when an organic phosphorus source was supplied. There was no significant difference in the growth and P uptake by chickpea between the treatments of phytate and KH2PO4 (Figs 2
–5). There have been reports of N transfer occurring in legume/cereal intercropping (Ta et al., 1989), but in the present study, sufficient N was added so that no nodules were found on the roots of chickpea. Thus, the improved growth of maize when intercropped with chickpea was not caused by better N nutrition. The improved growth of intercropped maize can be attributed to an improved P uptake. First, in hydroponics P concentration and P uptake of the intercropped maize supplied with phytate were significantly higher than in the case of the monoculture (Fig. 4). In contrast the P concentration of the intercropped chickpea was lower than monoculture culture when phytate was supplied (Fig. 4). Secondly, in soil culture when chickpea and maize grew together, total P uptake by maize was higher with no root barrier than with solid barrier (Table 1). Because of the competition of maize roots, part of P hydrolysed from phytate appeared to be taken up by the intercropped maize, resulting in its increased growth compared with monoculture plants.
Similar facilitation in P nutrition has been found in wheat/lupin associations (Horst and Waschkies, 1987; Kamh et al., 1999), sorghum/pigeon pea (Ae et al., 1990) and maize/groundnut intercropping (El Dessoug et al., 2003). However, such interspecific facilitation was not observed when maize was intercropped with sugar beet and oilseed rape (El Dessougi et al., 2003). In those studies, facilitation in P nutrition was focused on inorganic P. Li et al. (2003a) reported that when phytate-P was supplied, the P concentrations in wheat (2·9 g kg–1 in shoots and 1·4 g kg–1 in roots) without a root barrier between wheat and chickpea were higher than those in the treatments with a nylon mesh or with a solid barrier separation (1·9 g kg–1 in shoots and 1·0 g kg–1 in roots). This result also indicated that chickpea could facilitate phosphorus nutrition in associated wheat under organic P supply conditions. However, the mechanism of the facilitation was unknown.
Phosphatase secreted by chickpea plays an important role in the improvement of maize phosphorus nutrition
For phosphates to be available to plants from phytate, it must be hydrolysed by phosphatase (Richardson et al., 2000). Plant roots with a high phosphatase activity have great potential to utilize soil organic phosphorus (Helal, 1990). Under conditions of P deficiency, acid phosphatase secreted from roots was increased (Nakas et al., 1987; Li et al., 1997; Hays et al., 1999). In the present study, it is clear that chickpea root was able to secret greater amounts of acid phosphatase in hydroponic (Fig. 6) culture and soil culture than maize (Fig. 7), and increased hydrolysis of phytate. As a result, chickpea could utilize phytate as effectively as KH2PO4 (Fig. 2; see also previous experiments; Li et al., 2003a). Although the acid phosphatase activity of maize roots also increased significantly when organic P was supplied or when no P was added, the enzyme secreted from maize roots was two to three times less than that from chickpea (Fig. 6). The species variation in acid phosphatase secretion and utilization of organic P confirmed previous reports. Li et al. (1997) observed that Brachiaria decumbens CIAT 606 had the highest acid phosphatase activity in 16 plant species either grown under P-sufficient condition or P-deficient condition. The amount of acid phosphatase secreted by legumes was 22 % higher than by oilseeds and 72 % higher than by cereals (Yadav and Tarafdar, 2001). Egyptian clover (Trifolium alexandrinnm; Tarafdar and Claassen, 1988) and agroforestry species (George et al., 2002a, b) with higher rhizosphere soil acid phosphatase activity could use organic P that was unavailable to maize. However, Furlani et al. (1987) noted phytin was not a preferred source of P for sorghum genotypes. In the present study, enhanced phosphatase activities were associated over time with chickpea but not maize (Fig. 6).
The ability of chickpea to mobilize organic P was greater than that of maize. This could be related to root exudation of protons and organic acids. The optimum pH for phosphatase activity was in the range of 5–6. But acid phosphatase activity is still very high at pH 5–8 (Mclachlan, 1980). Rape roots reduced the rhizosphere soil pH from 6·7 to 5·5 (Gahoonia and Nielsen, 1982). Evidently chickpea releases considerable amounts of organic anions in response to phosphorus deficiency, and can lower the rhizosphere soil pH from 6·5 to 5·5 (Stevens, 2000). In the present study, the pH in the rhizosphere of chickpea was also lower than that of maize (data not shown), the condition conducive to hydrolysis of organic P by acid phosphatase. In a P-deficient sandy soil, more inorganic P was liberated by simultaneous application of acid phosphatase and organic acids identified in the rhizosphere solution of Hakea undulata than by the separate application of organic acid or acid phosphatase (Neumann and Romheld, 2000). An alternative function of root-secreted acid phosphatase may be the rapid retrieval of P by the hydrolysis of organic P, which is permanently lost by diffusion or from sloughed off and damaged root cells (Lefebvre et al., 1990). Further, soil pH may affect the sorption of the enzymes and the effect of pH on sorption of enzymes has only recently been realized as being important in measurement of phosphatase activity.
Root length
The size of the root system is one of factors that determines P uptake. Because of its low mobility in soil, P transport to the root surface is mainly governed by diffusion (Barber, 1995). An extensive root system with fine roots is beneficial for accessing a large soil volume. In the intercropping system, the roots of maize and chickpea were mixed together, so phosphate hydrolysed from phytate by chickpea could be absorbed by maize. The increased root length of intercropped maize might contribute to the increased total P uptake in maize. In another study, maize intercropped with groundnut produced more than double the root length of mono-cropped maize at no P (El Dessougi et al., 2003). The reason for this is unknown.
In conclusion, the increase in total P uptake by maize when intercropped with chickpea indicated that at limited P supply, intercropping can contribute to a more efficient utilization of organic P in soil by less P-efficient crops. This occurs because of exudation of P-mobilizing compounds by the roots of P-efficient plant species. To date there is no direct evidence that phosphatase activity produced by chickpea enhances the mineralization of organic P and absorption by associated maize at the field level. Future work should compare the effects of growing normal chickpea and mutants defective in phosphatase activity on the mineralization of soil organic P and P uptake by associated maize.
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ACKNOWLEDGEMENTS |
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The study was supported by the Major State Basic Research Development Program (Project number G1999011707), and the National Natural Science Foundation of China (Project number 30070450).
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