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Soil Science Society of America Journal 64:1644-1650 (2000)
© 2000 Soil Science Society of America

DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY

Rhizobia Inoculation Improves Nutrient Uptake and Growth of Lowland Rice

J.C. Biswasa, J.K. Ladhaa and F.B. Dazzob

a Soil Microbiology Lab., Soil and Water Sciences Division, IRRI, P.O. Box 3127, Makati Central Post Office, 1271 Makati City, Philippines
b Dep. of Microbiology, Michigan State Univ., East Lansing, MI USA

j.k.ladha{at}cgiar.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 Materials and methods
 Results and discussion
 Conclusions
 REFERENCES
 
Growth-promoting diazotrophs can enhance the growth and development of associated crops by transferring fixed N or by improving nutrient uptake through modulation of hormone-linked phenomena in inoculated plants. Six rhizobial diazotrophs isolated from a wide range of legume hosts were investigated to determine their growth-promoting activities in lowland rice (Oryza sativa L.) during 1997. Seeds and seedlings of rice Pankaj were inoculated with different rhizobia and grown in potted soil supplemented with varied amounts of mineral N. Inoculation with Rhizobium leguminosarum bv. trifolii E11, Rhizobium sp. IRBG74, and Bradyrhizobium sp. IRBG271 increased rice grain and straw yields by 8 to 22 and 4 to 19%, respectively, at different N rates. Nitrogen, P, and K uptake were increased by 10 to 28% due to rhizobial inoculation. Nitrogen-15-based studies indicated that the increased N uptake was not due to biological N2 fixation (BNF). Inoculation also increased Fe uptake in rice by 15 to 64%. Indole-3-acetic acid (IAA) accumulated in the external root environment of rice plants when grown gnotobiotically with rhizobia. The results indicate that certain strains of rhizobia can promote rice growth and yield, most likely through mechanisms that involve changes in growth physiology or root morphology rather than BNF.

Abbreviations: ANUE, agronomic N-use efficiency • BNF, biological N2 fixation • CFU, colony-forming units • DAI, days after inoculation • DAT, days after transplanting • IAA, indole-3-acetic acid • PGPR, plant growth-promoting rhizobacteria • RP-HPLC, reverse-phase high performance liquid chromatography • YM, yeast mannitol


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
Materials and methods
 Results and discussion
 Conclusions
 REFERENCES
 
ABOUT 2.4 BILLION PEOPLE worldwide depend on rice as their staple food (IRRI, 1996). Demand for rice is increasing, thus requiring growers to use additional nutrient inputs, especially mineral N, to increase yield. Higher N application may result in NO-3 pollution of groundwater (Mytton, 1993; Shrestha and Ladha, 1998), soil acidification (Kennedy and Tchan, 1992), and increased denitrification resulting in higher emission of N2O to the atmosphere, which may impact global warming (Bronson et al., 1997). In addition, the burning of fossil fuel to manufacture N fertilizers is a source of hazardous byproducts that pose a threat to human health and the environment (Vitousek et al., 1997). These problems have renewed public interest in exploring alternate or supplementary nonpolluting sources of N for agriculture (Ladha et al., 1997).

Traditional sources of organic N fertilizers are green manure, farmyard manure, and night soil, but farmers are reluctant to use these organic sources because of their associated management problems and higher costs compared with mineral N fertilizers. Although the use of mineral N fertilizer in rice production has increased substantially, its (agronomic) use efficiency is <50%. More than one-half of the applied N is lost through various processes, resulting in higher production costs and considerable environmental pollution (Ladha et al., 1998a). Two potential approaches are being explored to solve this problem. One is to create rice plants that can fix their own N (Ladha and Reddy, 1995). The other is to improve the uptake of native soil N and applied N by rice plants (Ladha et al., 1998a). The first approach is a long-term strategy that should continue to be pursued, but equally important is the search for short-term avenues to improve N-use efficiency in rice production. Nutrient uptake and nutrient use efficiency in crop plants can be manipulated by varying the source, timing, and amount of fertilizers; by adding organic materials; and by inoculating with plant growth-promoting rhizobacteria (PGPR). Most inoculation studies have focused on free-living diazotrophs, although a few reports indicate rhizobia can act as PGPR (Hoflich et al., 1995; Noel et al., 1996; Yanni et al., 1997). The PGPR influence crop growth and development by changing the physiological status (Glick and Bashan, 1997; Volpin and Phillips, 1998) and morphological characteristics of inoculated roots (Noel et al., 1996; Yanni et al., 1997; Biswas, 1998) which favor improved nutrient uptake (Okon and Kapulnik, 1986). The growth-promoting effects of rhizobacteria may include phytohormone production (Tien et al., 1979; Hussain et al., 1987; Chabot et al., 1996), fungal growth inhibition (Nautiyal, 1997), N2 fixation (Urquiaga et al., 1992), more efficient use of N sources (Yanni et al., 1997) and other nutrients (Chabot et al., 1996), antibiosis against phytopathogens (Handlesman and Staab, 1996), production and secretion of siderophores (Neilands and Leong, 1986), and induction of systemic disease resistance (Tuzun and Kloepper, 1994).

Associative and endophytic N2 fixation have been reported in graminaceous plants with free-living diazotrophs (Urquiaga et al., 1992; Lee et al., 1994; Shrestha and Ladha, 1996). Recently, Yanni et al. (1997) and Biswas (1998) reported increased N uptake by rice plants inoculated with rhizobia. This plant response is significant because of its potential importance to sustainable agriculture, especially in cropping systems involving rotations of rice and legumes. It raises questions of whether this benefit of rhizobia to rice may be due to their associative N2 fixing activity and/or their ability to change the phytohormone balance, thereby influencing growth physiology in ways that affect major nutrient uptake in rice. This study was undertaken (i) to investigate the ability of rhizobia to promote growth, seed production, and efficient uptake of mineral N, P, K, and Fe by lowland rice, and (ii) to assess the potential for BNF and auxin production as possible mechanisms of plant growth promotion in this beneficial rhizobia–rice association.


   Materials and methods
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
Results and discussion
 Conclusions
 REFERENCES
 
Experimental Detail
Two greenhouse experiments were conducted in 1997 at IRRI, Los Baños, Philippines, in a completely randomized design with eight replications. Effective rhizobial strains (see below) and N rates (0, 30, and 60 mg N kg-1 soil) were used as treatments. `Pankaj', a traditional rice cultivar (growth duration, 125 d) previously found to support high associative N2 fixation under greenhouse conditions (Shrestha and Ladha, 1996), was used as the test plant. Initially, six inoculant strains covering a range of legume hosts (Rhizobium leguminosarum bv. trifolii E11 and E12 nodulating Trifolium alexandrinum L. (Linneaeus), Bradyrhizobium elkanii (previously B. japonicum) USDA94 nodulating Glycine max (L.) Merr., Bradyrhizobium sp. IRBG271 nodulating Aeschyneomene fluminensis Vell, Rhizobium sp. IRBG74 nodulating Sesbania cannabina Linn. & Merrill and Rhizobium sp. Tal441 nodulating Vigna radiata (L.) Wilez. were selected based on prior knowledge of their association with and growth promotion of rice, and their production of phytohormone(s) (Biswas, 1998; Yanni et al., 1997). The three strains (E11, IRBG74, and IRBG271) found in Exp. 1 to significantly increase grain yield when inoculated with a supplement of 30 mg N kg-1 soil, were then reevaluated in Exp. 2 using supplementary N at 30 and 60 mg N kg-1 soil.

Maahas clay soil (isohyperthermic Andaqueptic Haplaquoll), previously amended with 15N-urea (Shrestha and Ladha, 1996), was used in both experiments. Initial soil properties were: pH (1:1 w/v water), 6.8; 15N atom% excess, 0.0697; organic C, 12.3 g kg-1; Olsen P, 30 mg kg-1; exchangeable K, 1.73 cmol kg-1; NH+4–N, 11 mg kg-1; total N, 1.09 g kg-1; electrical conductivity (1:1), 0.23 dS m-1; and cation-exchange capacity, 30 cmol kg-1. Ammonium in KCl extracts was measured by steam distillation methods (Bremner and Keeney, 1965). Active Fe was measured by the method of Asami and Kumada (1959).

Finely ground, air-dried soil was thoroughly mixed with fertilizers before addition to pots (9 kg soil pot-1). Each kilogram of potted soil received 22.5 mg P as NaH2PO4·H2O, 16 mg K as KCl, and 5 mg Zn as ZnSO4 1 d before transplanting. One-third of the fertilizer N (certified urea) was added just before transplanting. The remaining N was applied in equal doses at 35 and 70 d after transplanting (DAT). Nonsterile potted soil was watered and puddled properly before planting on 16 January for Exp. 1 and on 10 Oct. 1997 for Exp. 2. Tapwater was added on alternate days to completely flood the potted soil. After Exp. 1, all potting soil was combined, mixed thoroughly, and reused in Exp. 2. The physicochemical properties of the soil described above did not differ in Exp. 1 and 2.

Preparation of Inocula, Inoculation, and Planting
Rhizobia and bradyrhizobia were grown in yeast mannitol (YM) broth (Somasegaran and Hoben, 1985) and in half-strength tryptone glucose yeast extract broth (BBL, Cockeysville, MD), respectively. Cells in the exponential phase were collected by centrifugation at 925 g for 10 min at 6°C, washed with sterile phosphate buffered saline (0.14 M NaCl, 0.003 M KCl, 0.005 M Na2HPO4, 0.002 M KH2PO4; pH 7.0), and recentrifuged. Bacterial inoculum was prepared by resuspending pelleted cells in xanthan gum (5 g L-1) solution at a concentration of 5 mL packed cell volume L-1. Rice seeds of uniform size were inoculated by dipping them into the bacterial suspension. Subsequently, seeds were dried at room temperature and bacterial counts were made using serial dilution plating onto YM agar. The mean inoculation level was 10-5 cells per seed. The inoculated seeds were imbibed on moist filter paper in petri dishes for 3 d, and the pregerminated seeds were transplanted into soil in plastic trays (14.5 by 28.5 by 33.5 cm) containing 6 kg of air-dried soil and grown for 22 d. At that time, one healthy seedling was transplanted per pot. Each seedling was reinoculated at the base of the plant with 1 mL of culture containing 106 colony forming units (CFU) at 20 DAT in Exp. 1 and at 10 DAT in Exp. 2. An equivalent number of dead bacterial cells of IRBG271 (autoclaved at 121°C and 103.5 KPa for 20 min) were added to each uninoculated control plant.

Measurement of Agronomic Characteristics
The grain yield (g pot-1) is reported at 140 g kg-1 moisture content. The straw yield was recorded after oven drying at 70°C for 3 d.

Nutrient Uptake
Plants for nutrient and 15N determination were sampled at harvest. Root, shoot, and grain were washed with tapwater followed by distilled water, and oven dried at 70°C for 3 d. Plant samples were ground in a Wiley Laboratory Mill (Model 4, Thomas Scientific, Philadelphia, PA), and reground in a Vibrating Sample Mill (Heiko T1-100, Heiko Seisakusho Ltd, Tokyo, Japan). The plant samples were analyzed for total N by a Dumas elemental analyzer (Roboprep-CN 7001, Europa Scientific Ltd., Cheshire, UK) and for 15N by a mass spectrometer (VG-Model 903 Stable Isotope Mass Spectrometer) at IRRI's Analytical Services Laboratory. Leaf samples collected at 80 DAT from Exp. 1 were analyzed for N using the PE 2400 CHN Analyzer (Perkin Elmer Corp., Norwalk, CT) (Jimenez and Ladha, 1993). Because the chlorophyll content at the middle portion of the rice leaf blade is highly correlated with its N concentration, plant N values in Exp. 2 were obtained indirectly by a nondestructive sampling technique (Ladha et al., 1998b) using the SPAD-502 chlorophyll meter (Minolta, K. Arano & Co. Ltd, Tokyo, Japan). The actual leaf N concentrations of Exp. 1 were used to develop a regression equation, Y = -13.145 + 0.82647X, R2 = 0.6350, where Y is the leaf N (g N kg-1) and X is the SPAD meter reading of the chlorophyll content in the leaves.

Physiological N-use efficiency (PNUE) and change in agronomic N-use efficiency ({Delta}ANUE) were determined as follows:

and


Plant P, K, and Fe were estimated by dry ashing, HCl extraction, and wet ashing methods, respectively (Yoshida et al., 1976), and calculated as milligrams per pot.

Estimation of Indole-3-Acetic Acid in Hydroponic Culture
All the operations for obtaining microbiologically controlled, hydroponic cultures of rice (except mechanical dehulling of seeds) were performed using sterile materials and aseptic technique at room temperature. Uniform grains were dehulled gently, treated with ethanol (700 mL L-1) for 3 min, rinsed three times with water, soaked for 3 min in a mixture of 1 g HgCl2 L-1 water and 30 mL NaOCl L-1 water, rinsed four times with water, soaked in water for an additional 4 h to completely remove sterilants, and finally washed four more times with water. Surface-sterilized seeds were germinated at 30°C on YM agar in the dark.

Hydroponic cultures were prepared using autoclaved test tubes (20 by 200 mm) containing an 8 by 1.5 cm strip of stainless steel mesh (size 20) positioned at the upper fluid level of 10 mL of Fahraeus N-free liquid plant growth medium (Fahraeus, 1957), all capped with silicon plugs. Two 1-d-old contamination-free seedlings were placed on the wire mesh at the meniscus level so that the roots would contact and grow into the medium. The roots of 4-d-old plants were inoculated with 1 mL of culture containing 106 CFU of E11, IRBG74, or IRBG271. Uninoculated plants were grown axenically as the control treatment. Ten tubes were used for each treatment. Enclosed tube cultures were grown in a growth chamber maintained with a 14-h light/10-h dark cycle at 27/25°C. At 5 and 10 d after inoculation (DAI), rice seedlings of five tubes of each inoculated and uninoculated treatments at each sampling time were removed. The hydroponic culture medium was collected individually from each tube, clarified by centrifugation at 925 g for 10 min at 10°C, and analyzed for IAA content by the colorimetric method of Gordon and Weber (1951), and by reverse-phase high performance liquid chromatography (RP-HPLC) (see below). Sterile Fahraeus medium was used as the blank. The experiment was performed twice.

For IAA analysis by RP-HPLC, filtered (0.22 µm) culture supernatants of hydroponic rice roots individually inoculated with E11 and IRBG74 were fractionated at room temperature on a µBondapak C18 reverse phase column (12.5-nm pore size, 10-µm particle size of packing material, 3.9 by 300 mm column; Waters Millipore, Milford, MA) equilibrated with 60:40 (v/v) acetonitrile/water. The flow rate and injection volumes were 0.8 mL min-1 and 50 µL, respectively. Indoleacetic acid in the column effluent was detected at 278 nm using a SPD-6A UV detector (Shimadzu, Kyoto, Japan), and quantitated by integration of the peak areas using a C-R6A Chromatopac system (Shimadzu) with calibrations made using authentic IAA (Sigma Chemical, St. Louis, MO) as standard. A comparison of the colorimetric and HPLC methods to measure the IAA content of a standard sample indicated that the two procedures were in fairly close agreement, with the latter overestimating the concentration by 4.5%.

Statistical Analyses
The data were analyzed by analysis of variances (ANOVA), and the means were compared following Fisher's test of least significant difference (LSD) to assess the effects of inoculation and N rates on rice yield and yield components.


   Results and discussion
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results and discussion
Conclusions
 REFERENCES
 
Yield of Rice
Rhizobial inoculation and N rates significantly influenced grain and straw yields of Pankaj rice in potted soil under greenhouse conditions. Among the six inoculant strains tested, E11, IRBG74, and IRBG271 significantly increased either grain or straw yields (Tables 1 and 2) . In Exp. 1 (Table 1), plants inoculated with either strain E11 or IRBG271 and receiving no fertilizer-N supplement produced a significantly higher grain yield (22 and 15% increases, respectively) as compared with the corresponding uninoculated control. Plants grown with a fertilizer supplement of 30 mg N kg-1 soil produced a grain yield that was significantly higher following inoculation with strains IRBG74 and IRBG271, as compared with the corresponding fertilized uninoculated control (Table 1). The mean straw yield of plants was significantly higher when inoculated with strain E11 and significantly lower when inoculated with strain USDA94 as compared with the uninoculated control (Table 1). When reevaluated in Exp. 2 (Table 2), inoculant strains E11, IRBG74, and IRBG271 significantly increased grain and straw yields of rice plants when provided with some fertilizer-N supplement, suggesting an interdependence of fertilizer-N inputs and inoculation for optimal gain in rice productivity. The yield-increasing plant components were panicles per pot and filled grains per panicle in both experiments (data not shown). Also, the total number of spikelets per plant at 60 mg N kg-1 soil was significantly higher when inoculated with either E11 or IRBG74 (data not shown).


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  		Table 1 Grain and straw yield of rice (cv. Pankaj) as influenced by rhizobial inoculation and N rates (Exp. 1)

 

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  		Table 2 Grain and straw yield of rice (cv. Pankaj) as influenced by rhizobial inoculation and N rates (Exp. 2)

 
Yanni et al. (1997) previously reported a higher grain yield when rice plants were inoculated individually with strains E11 and E12 in the presence of higher N rates. These earlier studies and the results reported here clearly indicate that rhizobial inoculation can enhance growth and productivity of rice, and that this beneficial effect is actually promoted rather than suppressed by fertilizer-N supplement. These results indicate that rice yield improvement from inoculation with rhizobia may be independent of BNF (described further below) and suggest that differences in yield were related to changes in growth physiology and/or root morphology of the rice plants (Yanni et al., 1997; Biswas, 1998; Volpin and Phillips, 1998).

Nitrogen Use Efficiency
No statistically significant change in physiological N-use efficiency occurred in rice as a result of rhizobial inoculation (data not shown), but {Delta}ANUE improved significantly when inoculated with certain rhizobial strains (Table 3) . The change in {Delta}ANUE was significantly improved at the lower N rate by inoculation with IRBG74, USDA94 and Tal 441 in Exp. 1 and with IRBG271 in Exp. 2. In comparison, all three test strains (E11, IRBG74, and IRBG271) improved {Delta}ANUE at the higher N rate (Exp. 2). Although strain E11 improved {Delta}ANUE only at the higher N rate in this study, a previous field inoculation trial conducted in the Nile delta indicated that strain E11 significantly improved ANUE of rice cultivar Giza-175 at one-third, two-thirds, and the full recommended rates of applied N (Yanni et al., 1997). These results indicate that the physiological status of rice may change because of inoculation with growth-promoting rhizobia, enabling the plant to make more efficient use of fertilizer-N inputs for seed production and thus favor improved grain filling.


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  		Table 3 Agronomic N use efficiency ({Delta}ANUE) as influenced by rhizobial inoculation and N rates in rice (cv. Pankaj)

 
Dinitrogen Fixation and Nutrient Uptake
The potential role of BNF in this beneficial rice-rhizobia association was investigated by 15N-based isotope dilution studies using inoculated plants grown in potted soil in the greenhouse. Under these conditions, inoculation had no influence on dilution of 15N in plants grown with any supplementary fertilizer-N in Exp. 1 (Table 4) . Although inoculation had significant effect on 15N atom % excess in Exp. 2, in all cases (except IRBG71) higher accumulation of plant 15N occurred, which was related to a larger amount of total N uptake by inoculated plants than that in the uninoculated control. Total accumulation of plant N was consistently and significantly higher (19–28% increase) when inoculated with strains E11, IRBG74, and IRBG271 at higher N rates (Fig. 1 and 2) . Leaf N concentration at the booting stage was also significantly higher in inoculated plants than in the corresponding uninoculated control in Exp. 1 (data not shown). Although inoculation with IRBG71 showed significantly lower 15N dilution, it represents only marginal N2 fixation (<4%). These results indicate that growth promotion and higher accumulation of plant N in rice following rhizobial inoculation is independent of BNF.


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  		Table 4 Nitrogen-15 atom % excess in whole rice (cv. Pankaj) plants as influenced by rhizobial inoculation and N rates

 


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  		Fig. 1 Nitrogen, P, K, and Fe uptake by rice plants (cv. Pankaj) as influenced by rhizobial inoculation and fertilizer N under greenhouse conditions (Exp. 1). Letters compare the means at P = 0.05 for a given treatment

 


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  		Fig. 2 Nitrogen, P, K, and Fe uptake by rice plants (cv. Pankaj) as influenced by rhizobial inoculation and fertilizer N under greenhouse conditions (Exp. 2). Letters compare the means at P = 0.05 for a given rate of N application

 
Phosphorus, K, and Fe uptake also increased significantly in Pankaj rice when inoculated with rhizobia and provided with supplementary N treatments (Fig. 1 and 2). Inoculation with test strains E11, IRBG74, and IRBG271 led to {approx}13 to 23% and 10 to 16% higher uptake of P and K, respectively, as compared with the uninoculated control. Strain E11 consistently and significantly increased Fe uptake. The increased uptake of P, K, and Fe was invariably associated with higher N rates in both experiments.

The higher nutrient uptake may be related to morphological changes in rice roots, especially increased root number, thickness, and length (Yanni et al., 1997; Biswas, 1998; Dazzo et al., 2000), due to inoculation with growth-promoting rhizobia. Higher K and Fe uptake are related to thicker roots (Barber, 1985). Rhizobial inoculants may also induce an increased number of root hairs and root laterals, thereby favoring higher nutrient uptake by exploration of a greater soil volume. Because certain strains of rhizobia are able to solubilize precipitated P compounds (Chabot et al., 1996; Dazzo et al., 2000) and produce high affinity Fe-chelating siderophores (Guerinot, 1991), the possible contribution of these activities in increasing the availability of rhizosphere P and Fe for uptake by plant roots needs to be explored. Another possibility is that the diazotrophs may promote plant production of high-affinity siderophores. This possibility is supported by the finding that increased uptake of K enhanced phytosiderophore production and Fe uptake in oat (Avena sativa L.) (Hughes et al., 1992). Mori et al. (1991) also identified phytosiderophore and organic acid-complexed Fe in the xylem sap of rice plants. More studies are necessary to explore these possible mechanisms for enhanced uptake of plant nutrients operative in the rhizobia–rice association.

Indole-3-Acetic Acid Production
Both the colorimetric and HPLC tests for IAA were positive in samples of the external rooting medium of rice cultured gnotobiotically with rhizobia. Quantitation by HPLC indicated an increased level of IAA in inoculated hydroponic rice cultures, equivalent to {approx}2 mg IAA L-1 (Fig. 3) . Other studies using combined gas chromatography–mass spectrometry have confirmed that strain E11 can produce IAA in vitro, and that axenically produced rice root exudate can significantly stimulate IAA production by this rhizobial strain under these growth conditions (Dazzo et al., 2000). Lebuhn and Hartmann (1993) also found higher auxin contents in rhizosphere soils harboring rhizobia. Considered collectively, these results indicate that rhizobial inoculation can change the levels of IAA-like hormones in the rice root environment, but the influence of IAA in soil grown plants would only be observed if they take up IAA from the soil before it is metabolized by other rhizosphere microorganisms. The findings of increased tiller production and yield of rice found in this greenhouse study are consistent with a change in hormonal balance caused by rhizobial inoculation.



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  		Fig. 3 Indole-3-acetic acid (IAA) concentration in the external rooting medium of rice (cv. Pankaj) grown in gnotobiotic culture with rhizobia. The values (A) were determined colorimetrically and (B) were determined by high performance liquid chromatography. DAI = days after inoculation. The error bar indicates the standard error of the means

 

   Conclusions
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results and discussion
 Conclusions
REFERENCES
 
Grain and straw yields increased consistently when inoculated with rhizobial strains E11, IRBG74, and IRBG271. Rhizobial inoculation also significantly increased uptake of N, P, K, and Fe by rice plants compared with uninoculated controls. Increased N uptake was not due to BNF. These positive growth responses of rice to rhizobial inoculation were enhanced rather than suppressed at higher levels of added N fertilizer. The concentration of IAA was increased in the rice root environment when inoculated with rhizobia. The results confirm earlier studies indicating that certain strains of rhizobia can promote rice growth and seed production, possibly through mechanisms that involve changes in growth physiology and root morphology rather than BNF. More rhizobial strains should be screened through laboratory and field experiments to exploit their potential as PGPR for sustainable rice production.


   ACKNOWLEDGMENTS
 
Portions of this work was supported by a grant from the German Agency for Technical Cooperation and from the United States–Egypt Science and Technology Joint Fund Project BIO2-001-017-98.

Received for publication April 14, 1999.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results and discussion
 Conclusions
 REFERENCES
 




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