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Published in Soil Sci. Soc. Am. J. 68:1890-1895 (2004).
© 2004 Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA

Division S-4—Soil Fertility & Plant Nutrition

Nitrogen Fertilization on Uptake of Soil Inorganic Phosphorus Fractions in the Wheat Root Zone

Fucang Zhanga,c,d, Shaozhong Kanga,b,*, Jianhua Zhanga,c,d, Renduo Zhanga,c,d and Fusheng Lie

a Key Lab. of Agricultural Soil and Water Engineering in Arid and Semiarid Areas, Northwest Science and Technology Univ. of Agriculture and Forestry, Yangling, Shaanxi, 712100, China
b College of Water Resources and Civil Engineering, China Agricultural Univ., Beijing, 100083, China
c Dep. of Biology, Hong Kong Baptist Univ., Kowloon Tong, Hong Kong
d State Key Lab. of Water Resources and Hydropower Engineering Science, Wuhan Univ., Wuhan 430072, China and Dep. of Renewable Resources, Univ. of Wyoming, Laramie, WY 82071-3354, USA
e Agricultural College, Guangxi University, Nanning, Guangxi, China, 530005

* Corresponding author (kangshaozhong{at}163.net)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION AND SUMMARY
 REFERENCES
 
Plant nutrient uptake from the soil is dependent on fertilizers applied, soil chemicals, and other factors. The purpose of this study is to quantify the effects of applied N fertilizers on P uptake by winter wheat (Triticum aestivum L.) and on the change of soil pH in the root zone related to reductions of inorganic P fractions in the rhizosphere soil. An experiment was conducted using different forms of N fertilizers (i.e., NH4+–N and NO3––N) with three N concentrations (0, 100, and 300 mg kg–1) applied in a calcareous soil. Biomass and total N uptake of the plant increased with the N concentrations and NH4+–N fertilizer resulted in a greater biomass than NO3––N nutrition. Total P uptake in the plant was also higher with NH4+–N fertilizer than with the NO3––N nutrition. Compared with the zero N treatment, the soil pH around the roots decreased by 0.30 and 0.65 units, respectively, with N treatments of 100 and 300 mg kg–1 of NH4+–N fertilizer. The amount of soil inorganic P fractions in the root zone decreased with increasing NH4+–N applied. The NO3––N treatments reduced rhizosphere acidification and had a less impact on the soil inorganic P fractions. The results suggest that enhancing rhizosphere acidification attributable to applications of NH4+–N fertilizer can increase P availability in calcareous soils for plant uptake.

Abbreviations: Al-P, sterretite • ANOVA, analysis of variance • Ca2–P, dicalcium phosphate • Ca8–P, octocalcium phosphate • Ca10–P, hydroxyapatite • Fe-P, tinticite • O-P, the occluded phosphate


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION AND SUMMARY
 REFERENCES
 
TO INCREASE GRAIN PRODUCTION, a large amount of N and P fertilizers is applied in the modern agricultural practices. In recent years, more attention has been paid to P fertilization. Numerous studies showed that high P application rates not only increase grain yields and quality but also relieve the drought problem by promoting a deeper and more extensive root system (Payne et al., 1992; Rodriguez et al., 1996; Singh and Sale, 2000). However, the low efficiency of plant P uptake is the main problem associated with P applications. In a region with calcareous soils, the problem intensifies because of the interactions between P, Ca, and Mg in such soils (Hinsinger, 2001). Enhancing the availability of soil inorganic P to plant uptake is an important research subject as well as with practical aspects.

Recent studies demonstrate that plants play an active role in modifying the soil environment for better plant uptake of minerals (Marschner, 1995; Sas et al., 2001; Hinsinger, 2001). Roots can induce rhizosphere pH changes (Hinsinger, 1998; Jaillard et al., 2001), resulting from the root release of H+ or OH–/HCO3– (Haynes, 1990), organic acid exudation (Jones, 1998), redox potential (Fischer et al., 1989; Hinsinger, 2001), and root exudates (Gollany et al., 1993). It should be noted that the pH changes might alter the availability of some inorganic nutrients. Acidification in the root zone can increase soil inorganic P uptake by plants such as rape, soybean and ryegrass (Jungk, 1986; Youssef and Chino, 1989; Gahoonai et al., 1992).

Changes of various forms of extractable P in the rhizosphere have been studied extensively, including water-soluble P (Morel and Hinsinger, 1999), Olsen-P (Gahoonia et al., 1992), resin-P (Zoysa et al., 1998), NaOH-P (Saleque and Kirk, 1995), and acid-soluble P (Hedley et al., 1994). Processes such as NH4+–N fertilization can induce a change of soil pH and P mobility, thus increase P uptake by plants (Gahoonia et al., 1992). Therefore, it is valuable to examine how fertilization processes affect soil inorganic P fractions in the rhizosphere.

Our objective for this study is to quantify the effect of two main forms of N fertilizers (NH4+–N and the NO3––N) on the rhizosphere acidification and on soil P fractions. Specifically, we want to relate the rhizosphere acidification process to the availability of various inorganic P fractions, such as Ca2–P (dicalcium phosphate), Ca8–P (octocalcium phosphate), Ca10–P (hydroxyapatite), Al-P (sterretite), Fe-P (tinticite), and O-P (the occluded phosphate). An experiment was conducted using different forms and concentrations of N in a calcareous soil with winter wheat, in which plant uptake of P is an acute problem (Wang et al., 2000).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION AND SUMMARY
 REFERENCES
 
A calcareous soil (Sierozems) was collected from the top 20 cm of a cultivated layer in the Experiment Station of Northwest Science and Technology University of Agriculture and Forestry. The calcareous soil is widely distributed in the Guanzhong Plain of Shaanxi Province, in Northwest China. The soil was air-dried and sieved using 1-mm mesh. The main chemical concentrations in the soil included 6.8 g kg–1 organic C (Nelson and Sommers, 1982), 52 g kg–1 free CaCO3 (Nelson, 1982), 0.7 g kg–1 total N, 1.34 g kg–1 total P, 4.1 mg P kg–1 (Olsen et al., 1954), and 40 mg K kg–1 (1 M CH3COONH4–extractable K at pH 7). Soil pH was 8.1 (1:2.5 soil/water suspension). The soil was classified as sandy clay loam with sand, silt, and clay contents of 50, 7, and 43%, respectively.

The soil was mixed with 100 mg P kg–1 of KH2PO4 and filled in a large pot. The soil in the pot equilibrated for 40 d at the soil moisture of field capacity. After 40 d, the soil in the pot was air-dried and sieved again with 1-mm mesh. The available P (Olsen-P) in the soil was measured as 23.6 mg kg–1. Soil N fertilizer treatments included NH4+–N and NO3––N. For the NH4+–N treatments, (NH4) 2SO4 was applied and mixed into the soil at concentrations of 100 and 300 mg N per kg of dry soil. Nitrification inhibitor (Gijsman, 1990), 2-chloro-6-trichloromethyl pyridine, was added in the soil at a rate of 15 mg kg–1 of dry soil. For the NO3––N treatments, the fertilizer KNO3 was mixed into the soil at concentrations of 100 and 300 mg N per kg of dry soil. For comparison, a reference treatment was set up with the soil without adding any N fertilizer.

Rhizobox was used to study the rhizosphere processes (Kuchenbuch and Jungk, 1982; Zoysa et al., 1997) (Fig. 1) . Fifteen rhizoboxes were prepared for the five treatments with three replicates. Each rhizobox consisted of upper and lower portions. Each portion was made of a PVC cylinder (a diameter of 7.7 cm and a height of 3 cm) and was covered at the bottom with nylon cloth (50-µm mesh) so that plant roots only grew in the upper cylinder. Based on a bulk density of 1.3 g cm–3, the treated soil was packed carefully into the upper and lower cylinders, which were then sealed together with plastic tape. The rhizoboxes were placed into a large container filled with sand. A water supply scoop was installed at the bottom of the sand container. A constant soil water content of the rhizoboxes was achieved using a Mariotte bottle that was collected with the water supply scoop and maintained a –1.0-cm water pressure (Fig. 1).



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  		Fig. 1. Schematic plot of rhizobox.

 
Ten wheat seeds were planted in the upper cylinder of each rhizobox. The large container with the rhizoboxes was put in a growth chamber (Canada Conviron company, E8H) under a light intensity near the natural light condition and with a controlled temperature of 20°C. The wheat emergence was quite uniform for all cylinders without thinning. The winter wheat did not show any symptoms of deficiency of other nutrients during the experimental period. After the plants grew in the growth chamber for 30 d and roots developed around the interface between the upper and lower portions, the two portions of each rhizobox were separated. The lower portions with soil were frozen at –15°C for 24 h and the frozen soil cores cut into 1-mm thick slices. The slice soil samples were then air-dried and passed 1-mm mesh. Soil pH was measured using a pH meter (Beckman, pH-10) in soil paste with a soil/water ratio of 1/2.5. The remaining soil in each slice was passed through a 0.25-mm sieve. The soil samples were analyzed using a sequential fractionation method developed for calcareous soils (Jiang and Gu, 1989; Samadi and Gilkes, 1998). Abbreviations of Ca2–P, Ca8–P, Al–P, Fe–P, O–P, and Ca10–P were used to represent the more complicated terms of 0.25 M NaHCO3–soluble P, 0.5 M CH3COONH4–soluble P, 0.5 M NH4F-soluble P, 0.1 M NaOH-Na2CO3–soluble P, occluded-P, and 0.25 M H2SO4–soluble P, respectively. The upper soil portion was washed to recover the whole wheat plant. Dry weights of the whole plant and separate parts (leaves and roots) were measured after the plant samples were oven-dried at 80°C for 48 h. The plant samples were digested for total N and total P determination. The N concentration in the plant was measured by Kjeldahl method digested in a sulfuric-salicylic acid mixture (Buresh et al., 1982). The P concentration was measured colorimetrically after wet-digestion with HNO3 and H2SO4 (Jones et al., 1991).

Effects of N fertilization treatments on wheat root uptake and concentration reductions in the soil of various P fractions were analyzed using ANOVA (Analysis of variance). Multiple comparisons among the treatments were characterized using the least significant differences (LSD). ANOVA and multiple comparisons were performed using the SAS software (SAS Institute, 1990).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION AND SUMMARY
 REFERENCES
 
Results from ANOVA showed that plant heights did not increase significantly with the different N concentrations as well as the N forms during the experimental period (Table 1). However, the mean dry weights of whole plant and root increased significantly in the N treatments compared with the N0 treatment. The highest increase in biomass production was in the 300 mg NH4+–N kg–1 treatment. The effect of N treatments on the total plant N uptake was similar to those on the dry weights of the whole plants and roots. In general, the total plant P uptake increased with the N concentrations. However, the total plant P uptake for the 100 mg N kg–1 NO3––N treatment was similar to that for the N0 treatment. The 300 mg NH4+–N kg–1 treatment had the most significant increase in the total plant P uptake, indicating that NH4+–N nutrition increased bioavailability of soil P to wheat. Similar responses were observed in other plants (Gahoonai et al., 1992; Zoysa et al., 1998).


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  		Table 1. Effects of N fertilization treatments on wheat growth and uptake of N and P. Nitrogen treatments included applications of three N concentrations (0, 100, and 300 mg N kg–1) with (NH4)2SO4 and KNO3 . Plants were harvested after 30 d growing in a growth chamber.{dagger}

 
The soil pH had the maximum changes at the soil–root interface (the bottom of upper portion of the rhizobox) and gradually approached the original soil pH as the distance from the interface increased (Fig. 2) . To view the change tendency better, fitting curves with exponential functions are also shown in the figures. For the N0 treatment, the maximum decrease of soil pH was 0.2 attributable to the root-induced acidification (Morel and Hinsinger, 1999; Jaillard et al., 2001). Ammonium fertilization significantly reduced soil pH within the rhizosphere with the maximum decreases of 0.30 and 0.65, respectively, for the 100 and 300 mg NH4+–N kg–1 treatments. Nitrate fertilization had an opposite effect on the soil pH in the rhizosphere. The 100 and 300 mg NO3––N kg–1 treatments resulted in maximum pH increases of 0.12 and 0.27 from the original soil pH, respectively.



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  		Fig. 2. The pH values in the rhizosphere soil versus distance from the soil–root interface with the different N treatments. The treatments included applications of three N concentrations (0, 100, 300 mg N kg–1) with (NH4)2SO4 and KNO3 .

 
The common soil inorganic P fractions are the different forms of Ca and P compounds (Ca-P fractions) (Chang and Jackson, 1957). According to chemical extractions, the Ca and P compounds can be classified as follows: Ca2–P, Ca8–P, and Ca10–P (Jiang and Gu, 1989). Figure 3 presents the spatial changes of Ca2–P and Ca8–P in the rhizosphere with the different concentrations and forms of N. The largest reductions occurred at the soil–root interface and the chemical concentrations gradually approached the original soil chemical concentrations (the N0 treatment) as the distance from the interface increased. Reductions of Ca2–P in the rhizosphere soil were most significant for the NH4+–N treatments. The Ca2–P reduction zones in the soil were within 5, 8, and 11 mm from the interface, respectively, for the treatments of 0, 100, and 300 mg N kg–1 of NH4+–N kg–1 (Fig. 3A). Compared with the original concentration of Ca2–P in the soil, the maximum relative reductions of Ca2–P in the rhizosphere were 28.5% [calculated from (13 – 9.3)/13 x 100%] and 38.8% for the 100 and 300 mg N kg–1 NH4+–N treatments, respectively. Compared with the NH4+–N treatments, the reductions of Ca2–P were much smaller for the NO3––N treatments. The difference of Ca2–P changes between the NH4+–N treatments and the NO3––N as well as N0 treatments is probably mainly attributable to the rhizosphere acidification, which increased plant P uptake from the soil (Table 1).



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  		Fig. 3. Concentrations of (A) Ca2–P and (B) Ca8–P extracted from the wheat rhizosphere soil with the different N treatments. The treatments included applications of three N concentrations (0, 100, 300 mg N kg–1) with (NH4)2SO4 and KNO3 .

 
Octocalcium phosphate is a product of the gradual transformation of Ca2–P when P fertilizer is applied into soils (Syers and Curtin, 1988). Reductions of Ca8–P in the rhizosphere soil with the NH4+–N treatments were larger than with the NO3––N treatments. The maximum relative reductions of Ca8–P at the soil–root interface were 22.5 and 32.0% for the 100 and 300 mg N kg–1 of NH4+–N treatments, respectively (Fig. 3B). On a relative basis, the extent of Ca8–P reductions was less than that of Ca2–P. Similar to Ca2–P, the difference of Ca8–P reductions between the NO3––N treatments and the N0 treatment is minor, which implies a lower plant uptake of the P fraction in such cases (Table 1).

Hydroxyapatite (Ca10–P) is the least soluble soil inorganic P, which transforms very slowly from a P fertilizer application in the soil (Lindsay et al., 1989). The concentrations of Ca10–P in the rhizosphere soil with the applications of different forms and concentrations of N fertilizers were similar and close to that in the original soil. The minor change of Ca10–P suggests that this P fraction is difficult to be utilized by plants in all cases.

Sterretite and Fe-P changes in the rhizosphere are shown in Fig. 4 for the different treatments. Similar to the changes of the Ca-P fractions, the largest reductions of Al-P and Fe-P occurred at the soil–root interface and gradually approached the original soil Al-P and Fe-P concentrations (concentrations of the N0 treatment). The reduction zones of Al-P and Fe-P in the soil extended to about 10 mm from the interface. Compared with the original soil Al-P concentration, the relative changes near the soil–root interface of the rhizosphere soil were 8.0, 11.7, and 16.3% for the treatments of 0, 100, and 300 mg N kg–1 NH4+–N, respectively (Fig. 4A). The relative reductions of Fe-P near the soil–root interface were 5.8, 9.3, and 13.7% for the treatments of 0, 100, and 300 mg N kg–1 NH4+–N, respectively (Fig. 4B). The changes of Al-P and Fe-P for the NH4+–N treatments were much larger than those for the NO3––N treatments. Previous results showed that solubility of Fe-P and Al-P increased with pH (3 to 6.5) in acid soils (Hinsinger, 2001), whereas our results provided some information for changes of Fe-P and Al-P with pH in a basic soil. The reductions of Al-P with the NH4+–N treatments were larger than those of Fe-P, indicating that potentially Al-P was more available to plant than Fe-P.



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  		Fig. 4. Concentrations of (A) Al-P and (B) Fe-P extracted from the wheat rhizosphere soil with the different N treatments. The treatments included applications of three N concentrations (0, 100, 300 mg N kg–1) with (NH4)2SO4 and KNO3 .

 
The O-P is the occluded fraction of soil inorganic P, produced from the long-time interaction between P fertilizer and the soil solid surface. There were no obvious changes of O-P in the rhizosphere soil with the different treatments. The result suggests that O-P is the P fraction with the lowest solubility in soil and least available for plant uptake.

Similar to the changes of P fractions in Fig. 3 and 4, the total soil inorganic P (or the sum of all inorganic P fractions) had the largest reductions at the soil–root interface. Except for the treatment of 300 mg N kg–1 NH4+–N, reductions of the total P for the other treatments mainly occurred within a 10-mm region from the soil–root interface (Fig. 5) . Reduction percentages of P fractions and total P from the rhizosphere soil with the different N treatments are summarized in Table 2. After 30 d of the experiment, the reductions of total P with the ammonium treatments were greater than those of treatments with nitrate or no fertilizer. For example, at the location of 1 mm from the soil–root interface, the reductions of total P were 3.4, 6.2, 7.4, 3.6, and 2.7%, respectively, for the N0 treatment, the 100 and 300 mg NH4+–N kg–1 treatments, and the 100 and 300 mg NO3––N kg–1 treatments. Based on the LSD value of 1.37%, the reductions of total P for the 100 and 300 mg NO3––N kg–1 treatments were not significantly different from that for the N0 treatment.



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  		Fig. 5. Concentrations of total P extracted from the wheat rhizosphere soil with the different N treatments. The treatments included applications of three N concentrations (0, 100, 300 mg N kg–1) with (NH4)2SO4 and KNO3 .

 

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  		Table 2. Reduction percentages of P fractions and total P measured from the wheat rhizosphere soil with three N treatments. Values shown are the mean and standard deviations (SD) in the rhizosphere soil (0–5 mm from the soil–root interface).

 
A comparison of four soil P fractions showed that the amount of changes decreased in the order of Ca2–P, Ca8–P, Al-P, and Fe-P. Presumably the amount of plant uptake should increase in the same order. There was no significant reduction of Ca10–P and O-P in the rhizosphere of wheat for any treatments of N fertilizer (Table 2). Generally, Olsen-P is an available inorganic P to plant (0.5 M NaHCO3–extractable P) in the soil. A relationship between available P and Ca2–P is expected because both forms are determined by NaHCO3 extraction, though the two extractions are determined under quite different conditions (Samadi and Gilkes, 1998). The available P (Olsen-P) is positively related to Ca2–P and Ca8–P, and negatively related to Fe-P, indicating that changes of total P in the soil attributable to plant uptake are mainly from Ca2–P then Ca8–P. Dicalcium phosphate accounts for a small portion of the total P in the soil, but has the maximum relative reduction comparing with other fractions (Table 2) and the change of Ca2–P with the NH4+–N fertilizer treatments was most profound.


   DISCUSSION AND SUMMARY
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION AND SUMMARY
REFERENCES
 
An experiment was conducted using two forms of N fertilizers (NH4+–N and NO3––N) with three N concentrations (0, 100, and 300 mg kg–1) applied to a calcareous soil growing winter wheat. Based on analyses of the experimental data, results showed that biomass, root growth, and total N uptake of wheat plant increased more significantly with the NH4+–N treatments than with the NO3––N treatments. The results were attributable to rhizosphere acidification by NH4+–N nutrition, which increased bioavailability of soil P to the plant. In turn, the high available P enhanced the plant growth. More P plant uptake was found for the NH4+–N treatments than for the NO3––N treatments, likely a result from the increase of soil P mobility to the plant roots. The effect of NH4+–N treatments may be attributed to an enhancement of the diffusive flux of phosphate from the soil toward plant roots (Gahoonia et al., 1992; Wilkinson et al., 2000), resulting in higher P dissolution, which can be concluded from higher reductions of Ca-P and total P in the soil. In addition, other mechanisms such as root growth and distributions of mono- and dihydrogen phosphate may promote the transfer of P from soil into plants in the presence of NH4+–N (Blair et al., 1971). In general, high soil pH and Ca concentrations reduce the efficiency of soil P fertilization, such as in the calcareous environment (Sharpley, 2000). By modifying soil pH, plant roots can shift the chemical equilibrium that determines the mobility and bioavailability of soil inorganic P (Hinsinger, 2001). Our results showed that there was a significant decrease in soil pH, at the maximum of 0.30 to 0.65 units compared with the original soil, when different concentrations of NH4+–N fertilizer were applied. Apparently the acidification in the rhizosphere soil related to NH4+–N fertilization increased the soil inorganic P mobility and uptake. On the other hand, soil pH increased with the NO3––N treatments.

Plant roots have the ability to acidify the rhizosphere soil and increase soil P uptake, and the acidification is particularly promoted by the source of NH4+–N fertilizer. In calcareous soils, where P was mainly bound to Ca, acidification of rhizosphere soil with NH4+–N enhanced the availability of calcium phosphates to plant uptake, leading a large reduction of Ca2–P and Ca8–P in the soil. Even for Al-P and Fe-P, mainly existing in acid soils, a considerable reduction of the fractions in the calcareous soil with the application of NH4+–N fertilizer. The increase mobility and uptake of soil inorganic P fractions such as Ca8–P, Al-P, and Fe-P, which have relatively low solubility in the soil, should be beneficial to the plant. Plants can use these fractions of soil inorganic P in the initial seedling period if NH4+–N fertilizer is applied. Therefore, applying NH4+–N fertilizer in calcareous soils has a potential to increase P availability.

Comparing the four soil P fractions showed that the reduction rates were in the order: Ca2–P > Ca8–P > Al-P > Fe-P. There was no significant change of Ca10–P and O-P in the rhizosphere of wheat for all the treatments of different forms and concentrations of N applications. This suggested that H+ released by plants as a consequence of the uptake of NH4+ was insufficient to dissolve these fractions of soil inorganic P.


   ACKNOWLEDGMENTS
 
This research was partly supported by grants from the Chinese National Natural Science Foundation (50339030), Visiting Scholar Foundation of Key Lab in University, and from RGC of Hong Kong University Grants Council (HKBU 2041/01M).

Received for publication February 24, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION AND SUMMARY
 REFERENCES
 




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