Published in Soil Sci. Soc. Am. J. 68:1445-1451 (2004).
© 2004 Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
DIVISION S-8—NUTRIENT MANAGEMENT & SOIL & PLANT ANALYSIS
Diagnosis of Sulfur Deficiency in Soybean using Seeds
Kiyoko Hitsudaa,*,
Gedi J. Sfredob and
Dirceu Klepkerb
a Crop Production & Environment Division, Japan International Research Center for Agricultural Sciences (JIRCAS), 1-1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan
b Soybean Research Center of the Brazilian Agricultural Research Corp. (EMBRAPA-CNPSo), Caixa Postal 231, CEP 86001-970, Londrina, PR, Brazil
* Corresponding author (koki5025{at}jircas.affrc.go.jp).
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ABSTRACT
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The objectives of this study were to obtain a reliable index for the evaluation of the S nutrition status in soybean [Glycine Max (L.) Merr.] and to identify the critical S level in relation to seed yield and quality. Two Oxisols were used: A-horizon soil from Serra dos Gerais, and A- and B-horizon soils from Sambaiba in Maranhão State, Brazil. Soybean plants in pots were grown in a greenhouse with the supply of 0 to 80 mg S kg–1 soil. The seed S concentration was a more reliable index of seed yield because of the higher correlation between S concentration and yield. In the plants with visible symptoms of S deficiency, the seeds contained 1.5 g S kg–1, and the seed yield was 60% of the control. Electrophoresis analysis indicated that the critical seed S concentration for deficiency of protein components was 2.0 g kg–1 when the yield was 80% of the control. The S concentration was 2.3 g kg–1 or higher for >90% yield when the composition of the protein components was identical with that in the original seeds obtained under sufficient S fertilization. We classified the S concentration in the seeds as: deficient (S < 1.5 g kg–1), very low (1.5 
S < 2.0 g kg–1), low (2.0 S < 2.3 g kg–1), and normal (2.3 g kg–1 S). Because of stable S concentration, easy sampling, and sufficient time for planning of fertilizer application for the subsequent cropping, seed analysis is preferable to leaf analysis.
Abbreviations: ICP, inductively coupled plasma
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INTRODUCTION
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SEVERAL PRELIMINARY STUDIES showed that acid soils of the Brazilian Cerrado region, where soybean cultivation is rapidly expanding, lack S (McClung et al., 1959). Although S deficiency was repeatedly confirmed in various crops and many trials were performed to assess soil S fertility, the results of such trials have seldom been applied for field management. This is because S easily leaches by precipitation and accumulates in lower soil layers (Friesen, 1991), making it difficult to obtain a representative soil sample. Therefore, the results from pot experiments or from a specific field cannot be applied to other field conditions. However, the difficulty in soil S fertility assessment had not been a serious problem for field management hitherto, because S had been added as a component of other fertilizers, especially phosphoric materials that are heavily applied in the Cerrado area. Therefore, S deficiency may have been alleviated without prior recognition, and the deficiency may have been sometimes confused with P deficiency. Recently, however, fertilizers with a higher purity that contain less S have often been used, and S deficiency has tended to occur more frequently than before. As a result, it is important to develop a method to evaluate more easily the S nutrition status in soybean for the producers.
Sulfur concentration in a specific plant part, such as a plant shoot or leaf for 90% of maximum yield by fitting the Mitscherlich function, was widely taken as the critical concentration (Zhao et al., 1996). This percentage, which was considered to be high enough to ensure product quality, may not reflect latent deficiency. Besides, the S concentration decreases markedly with plant age, as does N concentration. Dijkshoorn and Lampe (1960) proposed the use of the S/N ratio in leaves as the S nutritional index, based on the concept that the ratio was constant in plant tissue proteins. Researchers adopted this proposal, converted the ratio into N/S to avoid decimal values, and examined the N/S ratio of many plants to evaluate S nutrition status. Nevertheless, Yoshida and Chaudhry (1979) showed that the N/S ratio in rice shoots was highest at 5 wk after transplanting, and then decreased over time. They reported that the use of the N/S ratio did not have any advantage over S analysis as diagnostic tool. Jones (1963) used the SO4–S concentration in grass leaves as an index of the S nutrition status because excess S accumulates as sulfate in plant tissues. Subsequently, Spencer et al. (1977) indicated that the SO4–S concentration changed considerably among plant parts and with plant age. To avoid the variation, Jones et al. (1980) adopted the SO4–S/S ratio in plant tops, and examined the critical value for subclover growth. However, analysis of two elements is more costly than single element analysis, and the indices controlled by two factors increased the risk of misinterpretation, as they required two kinds of chemical analysis. The use of two-factor indices does not enable readily assessment of plant growth and to determine the amount of each fertilizer for application. Furthermore, the indices may not reflect the critical values, and they may only indicate definitely sufficient or deficient conditions. These hold true for other multi-factorial criteria that require large databases.
Sulfur is one of the components of amino acids in seeds, including methionine and cysteine. Methionine is especially important as one of the essential amino acids for nonruminant animals, and it determines the nutritive value of foodstuffs. Sulfur accumulated during the vegetative stage is not substantially translocated into soybean seed. Sexton et al. (1998) indicated that S absorbed during the reproductive stage was mainly transformed into seed protein and that the transformation continued until the late seed filling stage. Sunarpi and Anderson (1997) showed that 87% of the seed S was absorbed during seed filling. Therefore, the diagnosis of soybean S deficiency based on the S concentration until the flowering stage does not enable determination of S sufficiency throughout the growth cycle to obtain a high quality seed product.
Once deficiency symptoms appear, crop yield markedly decreases. Even when the yield depression is not remarkable, product quality may suffer. In field management, it is important to prevent latent deficiency, and to determine the critical value of a deficient element for efficient fertilizer management. Previous reports showed that variations in S concentrations with plant age should be avoided, to obtain indices for the diagnosis of the S nutrition status in plants. A simple and reliable method of evaluating the S nutrition status in relation to soybean yield and seed quality should thus be developed. The objectives of this study were: (i) to develop an index for the determination of the status of S nutrition in soybean, and (ii) to identify the critical level of S in relation to soybean yield and quality.
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MATERIALS AND METHODS
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Soils Used
Two native Cerrado soils (Oxisols) occurring in the southern part of Maranhão State, Brazil, were used: a clay from Serra dos Gerais (Gerais) obtained from an A horizon (0–7 cm), and sandy clay loam samples from Sambaiba obtained from A and B (7–25 cm) horizons. The soils were analyzed for pH in water and in 0.01 M CaCl2 (soil/solution = 1:2.5, v/v); exchangeable acidity by the SMP-single buffer method (Shoemaker et al., 1961); total C concentration (Tyurin, 1931); exchangeable Al, Ca, and Mg concentrations by 1.0 M KCl extraction; available P and K concentrations by Mehlich-I extraction; and SO4–S concentration by 0.01 M Ca(H2PO4)2 extraction. The concentrations of all the inorganic elements were determined by inductively coupled plasma (ICP).
The 0- to 5-, 5- to 10-, 10- to 15-, 15- to 20-, 20- to 25-, and 45- to 50-cm horizons of native soil, and nearby soil cultivated for almost 20 yr at Sambaiba were sampled using a 100-cm3 cylinder, 5 cm high. In Gerais, similar sampling was performed only for the native soil, because of the absence of cultivated fields. The sampling was duplicated at the same pedon. The soil SO4–S concentration was determined by the method mentioned above.
Soybean Growth Response to the Application of Different Sulfur Levels
Native soils from the A horizon of Gerais (Gerais-A soil), as well as Sambaiba-A and Sambaiba-B soils were used to grow soybean. Sulfur was applied at rates of 0.0, 2.5, 5.0, 10.0, 20.0, 40.0, and 80.0 mg kg–1 dry soil as (NH4)2SO4, by equalizing the N amount with NH4NO3. The soil pH in water in each treatment was corrected to 5.5 with CaCO3 and MgCO3 (2:1). Four kilograms of soils were placed in plant pots, and four soybean seeds (cv. Patí) per pot were sown after Bradyrhizobium inoculation in a greenhouse of the Soybean Research Center, Brazilian Agricultural Research Corp. (EMBRAPA-CNPSo), Londrina, PR, Brazil. Each treatment was replicated six times.
The plants were watered with distilled and deionized water, and a S-free nutrient solution was irrigated depending on plant growth with an equal amount for all the treatments. The solution contained 167 mg N L–1 including 111 mg L–1 as Ca(NO3)2 · 4H2O and 56 mg L–1 as Mg(NO3)2 · 6H2O; 30 mg P L–1 as KH2PO4; 78 mg K L–1 including 38 mg L–1 as KH2PO4 and 40 mg L–1 as KCl; 160 mg Ca L–1 as Ca(NO3)2 · 4H2O; 48mg Mg L–1 as Mg(NO3)2 · 6H2O; 1.0mg Mn L–1 as MnCl2 · 4H2O; 0.2 mg Zn L–1 as Zn(C2H3O2)2 · 2H2O; 0.01 mg Cu L–1 as CuCl2 · 2H2O; 2.0 mg Fe L–1 as EDTA-Fe; 0.5 mg B L–1 as H3BO3; and 0.005 mg Mo L–1 as (NH4)6Mo7O24 · 4H2O. The solution pH was adjusted to 5.5 with NaOH or HCl. Supplementary KH2PO4 (0.50 g pot–1) was applied at the time of sowing and flowering.
The color of the third leaf from the top in four plants per pot was evaluated with a chlorophyll gauge meter (SPAD-520, MINOLTA Co., Ltd.) at flowering (70 d after sowing). Two plants were collected before supplemental addition of KH2PO4 to obtain the dry matter weight and to perform chemical analyses of the third leaf without petiole. In the A horizons of the Gerais and Sambaiba soils, the main stem leaves were separately sampled up to the tenth position from the top, and the S concentration was analyzed. Average S concentrations in leaves at each position were calculated from the concentrations under full S level treatments in both soils, and the relative concentration was obtained, taking the third leaf concentration as 100%. Two plants per pot were grown over the whole cycle (134 d) to obtain the seed yield and the nutrient element composition. Plant shoot dry weight at flowering and seed yield under the maximum S treatment in each soil were taken as control (100% reference). The plant tissue N was analyzed by the Kjeldahl method. After wet-ashing with HNO3 and HClO4, the concentrations of P, K, Ca, Mg, S, Fe, Mn, and Mo in leaf and seed were determined by ICP.
The composition of the protein components of the seeds was determined for ß-conglycinin and glycinin subunits by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) (Laemmli, 1970), compared with that of the original seeds cultivated with sufficient fertilization in a Maranhão field.
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RESULTS
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Chemical Properties of Soils Used
The pH values in water of the original soils ranged from 5.0 to 5.2 (Table 1). The concentrations of total C and SO4–S were in the order of Sambaiba-B < Sambaiba-A < Gerais-A. The concentrations of the other elements are presented in Table 1.
In the native soils, the concentration of SO4–S ranged from 2.7 to 4.3 mg kg–1 with small variations among the layers. In the cultivated field, however, the concentrations increased markedly with increasing soil depth from 2.9 to 19.5 mg kg–1 (Fig. 1).
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Fig. 1. Sulfate-S distribution in the layers of (a) native Gerais soil, (b) native Sambaiba soil, and (c) cultivated Sambaiba soil. Bars indicate standard errors (n = 2).
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Plant Growth and Grain Yield
Yellowing of the leaves was observed at flowering in the 0- to 5-mg S kg–1 soil treatments in the Sambaiba-A and -B soils, and in the 0-mg S kg–1 treatment in the Gerais-A soil; the plant leaves from higher positions slowly turned yellow, and stopped growing, resulting in smaller leaves and fewer branches. Subsequently, brown spots were observed on the edges of the leaves and on the pods. The values of the leaf color index in the third leaf at flowering ranged from 29 to 47, and yellowing could be visually detected for values <40. The different soils and S treatment significantly (P < 0.01) affected plant shoot dry weight at flowering and seed yield at harvest, but the interaction effect of both factors was not significant. The plant shoot weight at flowering was in the order: Sambaiba-B < Gerais-A < Sambaiba-A (data not shown). The plant shoot weight in the Sambaiba-A and -B soils increased with S application and the weight with <2.5 mg S kg–1 applied was significantly lower than the maximum weight obtained in the highest S level treatment of each soil. The plant shoot weight in the Gerais-A soil was almost constant regardless of the S level. The seed yield in the tested soils increased with S application up to the 20 mg S kg–1 soil treatment at least, and then almost reached a plateau (Fig. 2). The seed yield among the soils was in the order of Sambaiba-B < Sambaiba-A < Gerais-A across the S application rates.
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Fig. 2. Seed yield in relation to S application in the A horizon of the Gerais soil and the A and B horizons of the Sambaiba soil. The data represent the average values with standard error for six replications.
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Element Concentrations in Soybean Plants
The plant leaves at a higher position tended to exhibit higher S concentrations than those at a lower position (Fig. 3). Once S deficiency occurred, the concentration of S in the leaves at a high position where the deficiency symptoms started markedly decreased, and finally the S concentration reached values of almost 1.1 g kg–1 at all positions. The S concentration in the third leaf at flowering and in seeds increased with increasing S application. The S concentration with maximum S application was 2.3 to 2.8 g kg–1 in the third leaf, and 2.4 to 3.0 g kg–1 in seeds (Fig. 4). The N concentration in the third leaf also increased with increasing S applied from 24 to 47 g kg–1, unlike that in seeds, which was almost constant with an average value of 65 g kg–1 (Fig. 4). The concentrations of the other elements were in the normal range in plant tissues.
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Fig. 3. Relative value of average S concentration in the leaves at each leaf position on the plant, at flowering (left), and S concentration at each leaf position on the S deficient and sufficient plants at the same time (right). The average S concentration was obtained from all S treatments in the A horizon of the Gerais and Sambaiba soils, and the concentration in the third leaf was taken as 100%. The S deficient plants were obtained from the 2.5 mg S kg–1 soil treatment in the A horizon of the Sambaiba soil, and the S sufficient plants were obtained from the 40 mg S kg–1 soil treatment in the A horizon of the Gerais soil. Bars indicate standard errors.
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Fig. 4. Relationship between S and N concentrations in the third leaf at flowering, and those in seeds at harvest.
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Electrophoresis analysis of the seeds showed that S application decreased the content of ß-conglycinin, especially that of the ß-subunit, and increased the content of glycinin (Fig. 5).
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Fig. 5. Protein distribution in soybean seeds with different S concentrations. Arrows indicate compared subunits.
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DISCUSSION
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Soil Sulfur Distribution
In the native Gerais and Sambaiba soils, the SO4–S concentration did not vary significantly among the layers at different depths (Fig. 1). In the cultivated field at Sambaiba where sulfuric materials had been applied for many years as a component of fertilizers, the SO4–S concentration of the surface soil was as low as that in the native soils, whereas the concentration was high in the deeper horizons. Sulfuric fertilizers are easily solubilized and leached by precipitation, and the sulfate materials tend to accumulate in the lower layers of acid soils. This phenomenon may account for the fact that S deficiency symptoms often disappear after plant growth for a certain period of time in cultivated fields: the deficiency is alleviated after the roots reach the layers with S accumulation. The variations in S concentrations within the soil layers were large and the contribution of each layer to plant growth could not be easily determined. The depth of the layer with S accumulation varied, depending on the soil characteristics and the climatic conditions (Acquaye and Beringer, 1989). Therefore, it is difficult to generalize a soil sampling method, and soil S assessment through routine soil analysis cannot be easily applied to cultivated fields.
Sulfur Concentration in the Third Leaf at Flowering
Sulfur concentration showed a positive linear relationship with N concentration in the third leaf at flowering (Fig. 4), suggesting that S controlled N utilization. Attempts have been made to use the N/S ratio in leaves as an index of S nutrition status in many plants, but the results were not sufficiently reliable, as reported by Zhao et al. (1996)(and 1997). In the present study, the N/S ratio in the third leaf showed a low correlation with the relative seed yield, as the relative seed yield varied from 40 to 100% at similar values of the ratio (Fig. 6). Therefore, the N/S ratio was not suitable for use as an index of the S nutrition status of soybean plants.
Visible symptoms of S deficiency of soybean plants were more closely related to the leaf color index in the third leaf than to the relative shoot dry weight at flowering (Fig. 7). The color index values increased with increasing S concentration, with maximum values at 2.2 g S kg–1, followed by a decrease. When leaf S concentration was >1.5 g kg–1 with a color index of >40, the color difference among the treatments could not be detected either from the regression curve or by observation. Consequently, the critical S concentration for the visual detection of S deficiency symptoms was considered to be 1.5 g kg–1 in the third leaf. Sulfur concentrations in the third leaf (x) and in seeds (y) were similar within the range from 1 to 3 g S kg–1 of the third leaf (y = 0.859x + 0.242, r2 = 0.669**). These findings indicated that the S concentration in the third leaf at flowering enabled prediction of seed S concentration at harvest, and the plant with the critical concentration for the visual detection of S deficiency produced seeds that contained similar S concentration.
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Fig. 7. Relative shoot dry weight and leaf color index at different S concentrations in the third leaf at flowering. Shoot dry weight with maximum S application in each tested soil was taken as control (100% reference).
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Average S concentration in the second leaf was 9% higher, and that in the fourth leaf was 4% lower than that in the third leaf (Fig. 3). The third leaf from the top at flowering is the last leaf to become mature, and is generally used for nutritional assessment of S in soybean together with other elements (EMBRAPA-CNPSo, 2001). However, it is not always easy to identify the last mature leaf in fields. Moreover, Fontanive et al. (1996) showed that S concentration in the last mature soybean leaf decreased with the plant age; the leaf S concentration decreased by 1 to 27% among six varieties during plant growth from the full bloom stage to the pod stage. It is difficult to obtain a large number of leaf samplings in fields within the same growth stage. The diagnosis by foliar analysis is thus associated with considerable variation because of the difficulty in sampling.
Sulfur Concentration in Seed and Soybean Yield
Seed yield was in the order of Sambaiba-B < Sambaiba-A < Gerais-A soils, regardless of the S application rate (Fig. 2), and the order corresponded to SO4–S and total C supply in the native soils (Table 1). The S concentration in seeds showed a curvilinear regression with the relative seed yield, and so did the S concentration in the third leaf (Fig. 8). The coefficient of determination (R2) for the regression curve between the S concentration in seeds and the relative seed yield was higher than that between the S concentration in the third leaf and the relative seed yield, indicating that S concentration in seeds was a more reliable index of S nutrition status in soybean than S concentration in the third leaf. This is because, presumably, variations in S concentration associated with leaf sampling did not occur. Seed sampling at harvest is much easier than third leaf sampling at flowering in fields. In addition, the use of seeds for the diagnosis of S deficiency facilitates the planning of fertilizer application for subsequent cropping. Seed S analysis is also less tedious than leaf analysis at flowering. In any case, seed analysis for monitoring the S nutrition status in soybean appears to be more suitable than third leaf analysis.
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Fig. 8. Relative seed yield versus S concentration of the third leaf at flowering (left), and to seeds at harvest (right). The seed yield was relative to the highest seed yield at the maximum S application rate in the respective soils.
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Seed Protein Quality
Sulfur fertility affects the amino acid composition in seeds, which determines their nutritive value. Sulfur application increased the content of glycinin, with higher levels of S-containing amino acids, and decreased the content of ß-conglycinin with low levels of S-containing amino acids (Fig. 5). Gayler and Sykes (1985) suggested that changes in the protein composition of seeds resulting from S application might be a more suitable indicator than the conventional indices used in the evaluation of S fertility. In seeds, N concentration did not vary among the S treatments, but the S concentration decreased with decreasing S rate (Fig. 4). This finding suggested that the concentration of the amino acids that did not contain S increased under lower S conditions so as to maintain the total protein concentration in seeds, as reported by Blagrove et al. (1976). To determine the effect of seed S concentration on seed protein composition, protein profiles of the cultivated seeds were compared with that of the original seeds grown in a S-sufficient field by electrophoretic analysis (Fig. 5). In the seeds with 1.3 to 1.7 g S kg–1, the content of ß-conglycinin (especially ß-subunit) was higher and that of glycinin (acidic-IIa and basic subunits) was lower than the contents in the original seeds with 4.1 g S kg–1. The seeds with 2.1 g S kg–1 in the Gerais-A soil displayed a similar ß-conglycinin profile to that of the original seeds, but still exhibited the S-deficient glycinin profile. The seeds with 2.0 g S kg–1 in the Sambaiba-A soil showed a S-deficient ß-conglycinin profile, but had a S-sufficient glycinin profile. Therefore, the amino acid composition in the seeds changed from the deficient pattern to the sufficient one at around 2.0 g S kg–1. The seed S concentration was 2.3 g kg–1 or higher in all the soils when the protein profile became identical with that of the original seeds.
Diagnosis of Sulfur Nutrition Status in Soybean Using Seed
Sulfur concentration in the third leaf and in seeds showed an almost identical variation, and the plant shoot growth with S concentrations from 2.0 to 2.3 g kg–1 in the third leaf did not differ from that of the control in each soil, as shown by the relative dry weight, which exceeded 90% (Fig. 7). Nevertheless, the relative seed yield with the same concentration range in seeds varied from 79 to 100% (Fig. 8). Therefore, the plant shoot growth seemed to be normal, but the seed yield was not stable enough, and the seed protein quality was intermediate between the S-deficient and sufficient seeds with S concentrations ranging from 2.0 to 2.3 g kg–1 (Fig. 5). The plants showed a latent deficiency in S within this concentration range.
The regression curve between seed S concentration and relative seed yield showed that the 1.5 g S kg–1 seed concentration, which was considered to be the critical concentration for the visual determination of deficiency symptoms, corresponded to 60% seed yield of the control (Fig. 8). The 2.0 g S kg–1 seed concentration as the limit for the latent deficiency condition corresponded to 80% seed yield. The 2.3 g S kg–1 seed concentration as the limit for standard seed protein quality corresponded to 90% relative yield. Based on these results, we classified the S concentration in seeds into the following categories: deficient (S < 1.5 g kg–1), very low (1.5 g kg–1 S < 2.0 g kg–1), low (2.0 g kg–1 S < 2.3 g kg–1), and normal (2.3 g kg–1 S). The toxic level, which seldom occurs in fields, was not determined.
The reported field data were summarized (Tanaka et al., 1993), and the diagnosis of the S level in the third soybean leaf was scored. Since the results of leaf analysis obtained in this study were consistent with that estimation widely adopted (EMBRAPA-CNPSo, 2001), it is considered that the results from this pot trial can be applied in fields, as reported in rice (Yoshida and Chaudhry, 1979). The difference in S levels among varieties differing in genetical background which grow under different agronomic and climatic conditions should be further considered.
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CONCLUSIONS
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The present study demonstrated that seed S analysis is a simple and reliable method for diagnosis of the S nutrition status in soybean. Moreover, it shed a new light on the S level criterion, including seed protein quality evaluation, and the S concentration range for latent deficiency was elucidated for the first time. Sulfur fertility cannot be easily determined through analysis of cultivated soil because of the large variations among the layers. Neither plant shoot growth nor the leaf color can predict latent deficiency. Therefore, seed analysis is indispensable to evaluate the S nutrition status of soybean, and sulfuric materials should be applied to keep the S concentration above 2.3 g kg–1 in seeds.
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ACKNOWLEDGMENTS
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We thank Dr. Noriharu Ae, National Institute for Agro-Environmental Sciences, Japan and Prof. Junichi Yamaguti, Hokkaido University, Japan, for their suggestions and comments on the paper. We also thank Mr. Akio Kikuchi, Japan International Research Center for Agricultural Sciences, Japan and Mr. Luciano José da Silva, Soybean Research Center of Brazilian Agricultural Research Corporation, Brazil, for the assistance in the electrophoresis analysis and for the glasshouse support, respectively.
Received for publication September 12, 2003.
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TOP
ABSTRACT
INTRODUCTION
