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CROP PHYSIOLOGY & METABOLISM

Ureide Accumulation in Response to Mn Nutrition by Eight Soybean Genotypes with N₂ Fixation Tolerance to Soil Drying

^a USDA-ARS, and Agronomy Physiology and Genetics Laboratory
^b Agronomy Dep., Agronomy Physiology and Genetics Laboratory, Univ. of Florida, P.O. Box 110965, Gainesville, FL 32611-0965

^* Corresponding author (trsincl{at}mail.ifas.ufl.edu)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
Nitrogen fixation in soybean (Glycine max Merr.) is especially sensitive to soil drying. The basis of this sensitivity appears to be related to the fact that ureides are transported from the nodules, and the ureide concentrations increase with water deficits in leaves resulting in an apparent feedback to nodules involving ureides that inhibit activity. Therefore, sustained ureide catabolism in the leaves under water deficit appears to be critical for N₂ fixation tolerance. Recently, eight plant introduction lines were identified that expressed substantial N₂ fixation tolerance of water deficits. The focus of this study was to explore the basis for the tolerance previously observed in the eight lines. Specifically, the objective of this study was to evaluate in these genotypes the dependence for ureide catabolism on allantoate amidinohydrolase, which in other cultivars appears to be related to N₂ fixation tolerance of water deficits. Since allantoate amidinohydrolase does not require Mn as a co-factor in contrast to the alternate enzyme for allantoic acid catabolism, ureide accumulation was measured in leaves of these genotypes after the plants were fed allantoic acid following growth on low Mn hydroponic solutions. This treatment confirmed that ureide accumulation was independent of Mn nutrition level in six of the eight tolerant lines. Ureide accumulation in PI 429328 was consistently the most insensitive to Mn nutrition level. Overall, these results indicated that ureide catabolism independent of Mn is active in six of the eight plant introduction lines identified to express N₂ fixation tolerance to soil drying.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
A DECREASE IN symbiotic N₂ fixation of soybean early in soil drying has been known for some time (Kuo and Boersma, 1971; Sprent, 1971). A number of field studies subsequently confirmed that N₂ fixation in soybean was more sensitive to soil drying than was mass accumulation, and that this sensitivity had a deleterious affect on yield potential (Serraj et al., 1999a). This sensitivity is not universal among grain legumes and appears to be a trait of those species that transport ureides (allantoin and allantoic acid) from the nodules to the shoot (Sinclair and Serraj, 1995).

Soybean genotypes have been identified, however, that express substantial tolerance of N₂ fixation to water deficit. Sall and Sinclair (1991) identified the cultivar Jackson as having N₂ fixation sensitivity to water deficit that was no worse than that of mass accumulation. This encouraged a screen of a large collection of soybean plant introduction lines (>3000 lines) in an effort to identify lines that exhibited N₂ fixation drought tolerance (Sinclair et al., 2000). That study resulted in the identification of eight plant introduction lines that had N₂ fixation that was more tolerant of soil drying than was leaf gas exchange. The basis of the N₂ fixation tolerance to water deficit in the eight selected PI lines is not known.

Recent studies have focused on ureide accumulation and feedback on nodule activity as being crucial in influencing soybean N₂ fixation activity. Dramatic accumulation of ureides in response to water deficits has been observed in shoots of soybean grown in controlled environments (deSilva et al., 1996; Serraj and Sinclair, 1996a) and in the field (Serraj et al., 1997; Purcell et al., 1998). Experiments in which ureide was fed to soybean plants showed that N₂ fixation activity was readily inhibited as a result of increased ureide concentrations in the plant (Serraj et al., 1999b; Vadez et al., 2000). Consequently, ureide accumulation as a result of a failure in ureide catabolism in the shoot was hypothesized as an explanation of N₂ fixation sensitivity in soybean to soil drying (Serraj et al., 1999a).

Two enzymes have been identified for catalyzing allantoic acid breakdown in soybean. Shelp and Ireland (1985) identified the catabolic enzyme in the cultivar Maple Arrow as allantoate amidinohydrolase (EC 3.5.3.4). Winkler et al. (1987) could not confirm this observation in the cultivar Williams and found instead that allantoate amidohydrolase (EC 3.5.3.9) catalyzed allantoic acid degradation. This second enzyme was found to require Mn as a cofactor (Winkler et al., 1987; Lukaszewski et al., 1992). On the basis of responses to Mn, Vadez and Sinclair (2000) subsequently concluded that these two cultivars, in fact, employed differing catabolic enzymes as originally reported, and that there was genetic variation in the Mn requirement involved in ureide degradation. Further, Vadez and Sinclair (2001a) reported that Maple Arrow, which had the enzyme seemingly not requiring Mn, expressed tolerance of N₂ fixation to water deficit and that Williams, which required Mn, had N₂ fixation sensitive to water deficits.

The possibility of differing catabolic enzymes for allantoic acid leading to differences in N₂ fixation sensitivity to water deficits opens the possibility of genotypic segregation based on ureide degradation characteristics. Ureide accumulation (Purcell et al., 2000) and degradation (Vadez and Sinclair, 2002) in the tolerant cultivar Jackson is insensitive to Mn concentration in the leaves, indicating the presence of allantoate amidinohydrolase. Further, Vadez and Sinclair (2001a) compared ureide accumulation in leaves of nine soybean cultivars with varying sensitivity of N₂ fixation to water deficit, including five of the genotypes identified as being very tolerant of soil drying, after growing them on nutrient solutions containing either 0- or 6.6-µM Mn. Ureide accumulation in leaves of four of the tolerant lines was insensitive to Mn in the nutrient solution and there was relatively low ureide accumulation even under a zero-Mn treatment. The fifth tolerant line (PI 507039), however, had a large accumulation of ureide under the zero-Mn treatment, but this line had especially poor plant growth under this treatment. In situ measurements of leaf ureide degradation in the nine cultivars grown on zero Mn (Vadez and Sinclair, 2001a) showed a trend of increased degradation rate associated with N₂ fixation tolerance, but the variability was high. Because these plants were supplied with no Mn and the growth was decreased in all cultivars, the results may have been confounded by inhibited plant growth, which could have had a negative influence on ureide catabolism.

Since allantoate amidinohydrolase activity might be associated with N₂ fixation tolerance to water deficit and response to Mn might be a key point of difference in discriminating between the enzymes for allantoic acid degradation, characterization of the eight tolerant PI lines identified by Sinclair et al. (2000) for response to Mn is likely to improve the understanding of the tolerance mechanism. The objective of this study was to evaluate the influence of Mn supply on ureide accumulation and degradation in leaves of the eight tolerant PI lines. These studies were done exclusively using hydroponic solutions with differing Mn levels since the genotypic response of N₂ fixation to soil drying has been fully documented. An initial study with a few lines grown on low Mn availability was undertaken to evaluate measurements of in situ leaf ureide degradation rates and of ureide accumulation on ureide feeding to the plant. Subsequently, two experiments were undertaken to measure ureide accumulation in response to Mn treatment with all eight tolerant PI lines plus several check lines.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
Initial Experiment
Four tolerant plant introductions (PI 222547, PI 374163, PI 423886, and PI 429328) plus the sensitive cultivar Biloxi (Serraj and Sinclair, 1996b) were used in an initial experiment to evaluate N₂ fixation traits in response to growth on hydroponic solutions containing either adequate Mn (6.6 µM) or deficient Mn (0.33 µM). The plants were arranged in a split plot design with the two Mn treatments as the main plots and eight replicate plants of each cultivar in a treatment. They were grown in a greenhouse with day/night temperatures of 28/20°C and a photoperiod of 14 h.

The plants were established by first germinating the seeds in soil inoculated with commercial inoculant (Nitragin Inc., Milwaukee, WI)¹. After 1 wk, the emerged seedlings were individually transferred to rubber stoppers on 1-L Erlenmeyer flasks containing the following nutrient solution: CaC1₂ (3.3 mM), MgSO₄ (2.05 mM), K₂SO₄ (1.25 mM), KH₂PO₄ (0.35 mM), H₃BO₃ (4 µM), ZnSO₄ (1.55 µM), CuSO₄ (1.55 µM), NaMoO₄ (0.12 µM), and FeEDTA (40 µM) (Drevon et al., 1988). Manganese was supplied in either sufficient concentration (6.6-µM MnSO₂) or deficient concentration (no Mn for the first 2 wk after transplanting and 0.33-µM MnSO₄ thereafter). The solution provided at transplanting contained 1-mM urea to facilitate early growth of the plants before nodules were established. After 2 wk, urea was removed from the nutrient solution and the solution was replaced once weekly. The pH of the solution was maintained close to 7.0 by adding 0.2 g L^-1 CaCO₃ and air was continuously bubbled through the solution at a flow rate of 2 L min^-1 (Serraj and Sinclair, 1996b). The volume of nutrient solution was maintained at 500 mL so that most of the nodules were above the nutrient solution.

Ureide Treatment
Five weeks after transplanting, 5-mM allantoic acid (Sigma Chemical Co., St. Louis, MO) was included in the nutrient solution of half the plants (i.e., four plants of each cultivar and Mn treatment) (Vadez and Sinclair, 2000). The flasks were weighed daily following the ureide treatment to estimate the daily loss of solution. The daily loss in solution as a result of plant transpiration, which was 150 to 200 mL, was replaced by adding distilled water to the solution. Consequently, as the treatment progressed the ureide concentration in the nutrient solution was decreased substantially.

Leaf disc samples were collected from both ureide-treated and untreated plants on Days 0, 1, 2, 3, and 4 after the addition of ureide. Each sample consisted of three 1.6-cm diameter discs that were obtained by removing a single disc from each blade of the topmost fully expanded leaf. Ureide extraction was done by adding 1 mL of 0.2 M NaOH to the leaf disc samples and boiling for 30 min. The samples were centrifuged and then stored in a freezer until ureide analysis could be completed. Ureide concentrations of the leaf discs were measured using a colorimetric method (Trijbels and Vogel, 1966).

Leaf Ureide Degradation
On Day 5 following the initiation of the ureide treatment, in situ leaf ureide degradation measurements (Vadez and Sinclair, 2000) were made for plants that had not been subjected to the addition of allantoic acid to the nutrient solution. Therefore, a leaf was harvested from each of four untreated plants for each cultivar and Mn treatment. The harvested leaf was the topmost fully expanded leaf, which had completed expansion above the one from which the leaf disc samples were being collected. These leaves were detached from the plant at the stem and the petioles of the leaves were placed in individual test tubes containing a 7.5-mM allantoic acid solution. The leaves were allowed to uptake this solution over a 13-h period under the combination of a metal halide and a sodium lamp (>500 µmol m^-2 s^-1, Sun-Brella, Environmental Growth Chambers, Chagrin Falls, OH). Following this incubation period, six leaf-disc samples were obtained from each leaf and placed in 2-mL extraction vials. Each leaf-disc sample consisted of three 1.6-cm diameter discs that were obtained from each of the blades of the leaf. The leaf-disc samples were incubated in the vials under the artificial light for 0, 1.25, 2.5, 3.75, 5.0, and 6.25 h. The incubation was stopped by adding 1 mL of 0.2 M NaOH to the vial and boiling for 30 min., which was the first step in ureide extraction. Ureide concentration was measured as described previously. A linear regression of ureide concentration against incubation time for the six vials from each leaf was done to estimate ureide degradation rate.

Following the collection of the leaves for ureide degradation on Day 5, all plants were harvested. The plants were cut at the cotyledonary node and each plant was separated into leaves, stem, nodules, and roots. The plant material was oven dried (80°C) and weighed.

Genotype Comparison
Two similar experiments were conducted to test the sensitivity to Mn in ureide accumulation among N₂ fixation tolerant genotypes. In each experiment, the eight soybean plant introductions identified by Sinclair et al. (2000) as having N₂ fixation tolerance to water deficits (PI 222547, PI 227557, PI 374163, PI 423886, PI 429328, PI 507039, PI 507414, and PI 578315B) plus Biloxi and Jackson were tested. In Exp. 1, cultivars Williams and Maple Arrow were also included. A split plot design was again used with two Mn treatments as the main plots. In Exp. 1, there were four replicate plants per Mn treatment, and in Exp. 2 the number of replicates was increased to six.

The plants were established and grown as described in the initial experiment. In these experiments, only ureide accumulation was measured in leaf discs on each day following ureide addition to the nutrient solution as done in the initial experiment. That is, leaf discs were harvested from the topmost fully expanded leaf on each plant at Days 0, 1, 2, 3, and 4 following the addition of ureide to the nutrient solution. In these experiments, however, 3-mM allantoic acid was added to the nutrient solution and the solution lost through transpiration was replenished on each day with the nutrient solution containing ureide.

Differences between the two Mn treatments within each genotype were tested using a t test. Duncan's new multiple range test (P 0.05) was used to test differences among genotypes within a Mn treatment.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
Initial Experiment
A key feature of this experiment was to induce a Mn deficiency for plants grown on hydroponic solution, but not subject the plants to the extreme of zero-Mn supply as done in our previous study (Vadez and Sinclair, 2001a). The use of a nutrient solution containing 0.33-µM Mn eliminated any obvious adverse effects on overall plant growth during 6 wk of growth. There was no statistical difference in plant mass accumulation between the 0.33- and 6.6-µM Mn treatments for any of the five tested cultivars (data not shown).

A substantial range of in situ leaf ureide degradation rates was observed among the five cultivars (Table 1). Under the 6.6-µM Mn treatment, statistical significance was found between the cultivar with the highest rate and the two cultivars with the lowest rates. Unfortunately, a statistical difference among genotypes was not established for the 0.33-µM Mn treatment. The high variability in leaf ureide degradation rates that were observed among plants within a cultivar and Mn treatment seemed to be a major factor in the failure to establish significance even though the range in mean values was quite large.

View larger version (26K): [in this window] [in a new window]   Fig. 1. Ureide concentration in leaves collected from PI 429328 and ‘Biloxi’ plants grown on nutrient solutions containing either 0.33- or 6.6-µM Mn in the preliminary experiment. On Day 0, a 5-mM ureide treatment was added to the nutrient solution of half the plants.

The data for leaf ureide concentrations for Days 2 and 3 were combined to calculate a mean ureide concentration for comparing cultivars. There was no difference among cultivars in leaf ureide concentration for plants grown on 6.6-µM Mn (Table 2). However, significant differences (P 0.05) were observed among cultivars in leaf ureide concentration for those plants grown on 0.33-µM Mn. Biloxi had the highest concentration and PI 429328 had the lowest. A difference in leaf ureide concentration between the two Mn treatments within a cultivar were found only for Biloxi (P 0.01) and PI 374163 (P 0.05).

Experiment 2 was essentially a repeat of Exp. 1, but the number of replicate plants was increased to six to increase the possibility of demonstrating significant differences in leaf ureide concentrations. Identical to Exp. 1, Biloxi and PI 507414 were the only genotypes that had significant differences in leaf ureide concentrations between the 0.33- and the 6.6-µM Mn treatment (Table 4).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
The objective of this research was to characterize the response to Mn of the eight genotypes that have been identified as expressing considerable tolerance of N₂ fixation to water deficit (Sinclair et al., 2000). An initial experiment was undertaken to test the methods for measuring the influence of Mn on ureide levels in the leaves. A hydroponic solution of 0.33-µM Mn was found sufficient to allow unsuppressed plant growth within the time frame of these experiments. Even though plant growth on 0.33-µM Mn was not different from adequate Mn, 0.33-µM Mn resulted in significantly inhibited ureide catabolism in the leaves of Biloxi, which was previously found to be dependent on Mn, presumably a cofactor for allantoate amidohydrolase (Vadez and Sinclair, 2001a).

Results from the initial experiment on in situ leaf degradation did not allow segregation among genotypes. While the degradation rate of Biloxi grown on 0.33-µM Mn was less than half of the other genotypes, the variability in the data precluded a conclusion that the capacity of Biloxi for ureide degradation was different from the other genotypes. Since this technique for assessing ureide degradation is quite laborious and the results were variable, this approach was not pursued in additional experiments.

Measurement of ureide concentration in leaves on Days 2 and 3 following the addition of allantoic acid to the hydroponic solution proved to be a relatively simple and an effective method for comparing genotypes. In all three experiments, leaf ureide concentrations of Biloxi were significantly greater in the 0.33-µM Mn treatment than in the 6.6-µM Mn treatment. Williams, which has been shown also to be a cultivar sensitive to water deficits (Vadez and Sinclair, 2001a), had in Exp. 1 a probability level of 0.055 that leaf ureide concentration in the 0.33-µM Mn treatment was greater than in the 6.6-µM Mn treatment. This evidence supports previous conclusions that the water-deficit sensitivity in Biloxi and Williams is associated with a dependence on Mn for ureide catabolism.

Aside from Biloxi and Williams, all other genotypes in this test had been identified as having N₂ fixation tolerant of water deficit (Sinclair et al., 2000). Except for PI 507414, leaf ureide accumulation in the leaves was independent of the Mn levels on which the plants were grown. This result indicates that except for PI 507414, these other genotypes are likely to rely on allantoate amidinohydrolase, which does not require Mn as a cofactor, as the enzyme for allantoic acid catabolism. The insensitivity of these genotypes to Mn was also indicated by the comparatively low leaf ureide concentrations following the ureide treatment for plants grown on 0.33-µM Mn.

The results for PI 507414 might indicate a special situation. Since leaf ureide concentrations in this genotype were sensitive to the Mn treatment, these results indicate a dependence on allantoate amidohydrolase for allantoic acid degradation. Nevertheless, the accumulation of ureides when grown on 0.33-µM Mn was not significantly greater than all of the other tolerant genotypes in Exp. 1 and no worse that four other plant introductions in Exp. 2. PI 507414, however, had N₂ fixation that was substantially less tolerant of soil drying than the other seven genotypes identified by Sinclair et al. (2000). Therefore, this genotype might be of particular interest as a case that is mainly dependent on allantoate amidohydrolase, but the enzyme seems to be able to sustain reasonable activity both when Mn availability is low and under drying soil.

PI 507039 may be another genotype of special interest because its responses to Mn were so dramatically different between Exp. 1 and 2. In our earlier study (Vadez and Sinclair, 2001a), PI 507039 had very high leaf ureide concentrations for a zero-Mn treatment after allantoic acid was added to the nutrient solution. Our previous conclusion was that these results were a result of decreased plant growth as a consequence of Mn deficiency. This explanation did not apply to Exp. 2, where there was no inhibited growth under the 0.33-µM Mn treatment. The basis for the inconsistent behavior of PI 507039 is unknown but likely worth further investigation because this genotype had the most tolerant N₂ fixation to soil drying of the eight selections (Sinclair et al., 2000).

Overall, these results support the hypothesis that those lines previously identified as having N₂ fixation tolerant of water deficit are generally not sensitive to Mn availability, which indicates a reliance on allantoate amidinohydrolase as the major enzyme for allantoic acid catabolism. This conclusion applies to Jackson, Maple Arrow, and seven of the tolerant genotypes. PI 429328, based on the results of the three experiments described here, was especially insensitive to Mn based on the lack of ureide accumulation in the leaves.

	NOTES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 
¹ Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the USDA and does not imply approval or the exclusion of other products that may also be suitable.

Received for publication July 16, 2001.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS NOTES RESULTS DISCUSSION REFERENCES

 

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• Drevon, J.-J., V.C. Kalia, M.O. Heckmann, and P. Pedelahore. 1988. In situ open flow assay of acetylene reduction activity by soybean root-nodules: Influence of acetylene and oxygen. Plant Physiol. Biochem. (Paris) 26:73–78.
• Kuo, T., and L. Boersma. 1971. Soil water suction and root temperature effects on nitrogen fixation in soybeans. Agron. J. 63:901–904.[Abstract/Free Full Text]
• Lukaszewski, K.M., D.G. Blevins, and D.D. Randall. 1992. Asparagine and boric acid cause allantoate accumulation in soybean leaves by inhibiting manganese-dependent allantoate amidohydrolase. Plant Physiol. 99:1670–1676.[Abstract/Free Full Text]
• Purcell, L.C., C.A. King, and R.A. Ball. 2000. Soybean cultivar differences in ureides and the relationship to drought tolerant nitrogen fixation and manganese nutrition. Crop Sci. 40:1062–1070.[Abstract/Free Full Text]
• Purcell, L.C., R. Serraj, M. deSilva, T.R. Sinclair, and S. Bona. 1998. Ureide concentration of field-grown soybean in response to drought and the relationship to nitrogen fixation. J. Plant Nutr. 21:949–966.[ISI]
• Sall, K., and T.R. Sinclair. 1991. Soybean genotypic differences in sensitivity of symbiotic nitrogen fixation to soil dehydration. Plant Soil 133:31–37.
• Serraj, R., S. Bona, L.C. Purcell, and T.R. Sinclair. 1997. Nitrogen fixation response to water-deficits in field-grown ‘Jackson’ soybean. Field Crops Res. 52:109–116.
• Serraj, R., and T.R. Sinclair. 1996a. Inhibition of nitrogenase activity and nodule oxygen permeability by water deficit. J. Exp. Bot. 47:1067–1073.
• Serraj, R., and T.R. Sinclair. 1996b. Processes contributing to N₂–fixation insensitivity to drought in the soybean cultivar Jackson. Crop Sci. 36:961–968.[Abstract/Free Full Text]
• Serraj, R., T.R. Sinclair, and L.C. Purcell. 1999a. Symbiotic N₂ fixation response to drought. J. Exp. Bot. 50:143–155.[Abstract/Free Full Text]
• Serraj, R., V. Vadez, R.F. Denison, and T.R. Sinclair. 1999b. Involvement of ureides in nitrogen fixation inhibition in soybean. Plant Physiol. 119:289–296.[Abstract/Free Full Text]
• Shelp, B.J., and R.J. Ireland. 1985. Ureide metabolism in leaves of nitrogen-fixing soybean plants. Plant Physiol. 77:779–783.[Abstract/Free Full Text]
• Sinclair, T.R., L.C. Purcell, V. Vadez, R. Serraj, C.A. King, and R. Nelson. 2000. Identification of soybean genotypes with N₂ fixation tolerance to water deficits. Crop Sci. 40:1803–1809.[Abstract/Free Full Text]
• Sinclair, T.R., and R. Serraj. 1995. Dinitrogen fixation sensitivity to drought among grain legume species. Nature (London) 378:344.
• Sprent, J.I. 1971. Effects of water stress on nitrogen fixation in root nodules. Plant Soil Special Vol. 225–228.
• Trijbels, F., and G.D. Vogel. 1966. Degradation of allantoin by Pseudomonas acidovirans. Biochim. Biophys. Acta 113:292–301.[Medline]
• Vadez, V., and T.R. Sinclair. 2000. Ureide degradation pathways in intact soybean leaves. J. Exp. Bot. 51:1459–1465.[Abstract/Free Full Text]
• Vadez, V., and T.R. Sinclair. 2001a. Leaf ureide degradation and N₂ fixation tolerance to water deficit in soybean. J. Exp. Bot. 52:153–159.[Abstract/Free Full Text]
• Vadez, V., and T.R. Sinclair. 2002. Sensitivity of N₂ fixation traits in soybean cultivar Jackson to manganese. Crop Sci. 42:791–796.[Abstract/Free Full Text]
• Vadez, V., T.R. Sinclair, and R. Serraj. 2000. Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N₂ fixation in soybean. Physiol. Plant. 110:215–223.
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This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (9) Citing Articles via Google Scholar Google Scholar Articles by Sinclair, T. R. Articles by Chenu, K. Search for Related Content PubMed Articles by Sinclair, T. R. Articles by Chenu, K. Agricola Articles by Sinclair, T. R. Articles by Chenu, K. Related Collections Soybean Crop Physiology & Metabolism Symbiosis