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Published online 27 October 2005
Published in Crop Sci 45:2497-2502 (2005)
© 2005 Crop Science Society of America
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CROP PHYSIOLOGY & METABOLISM

Nitrogen Fixation, Amino Acid, and Ureide Associations in Chickpea

Dil Thavarajaha, Rosalind A. Balla,* and Jeff J. Schoenaub

a Department of Plant Sciences, University of Saskatchewan, 51 Campus Dr., Saskatoon, Saskatchewan, Canada S7N5A8
b Department of Soil Science, University of Saskatchewan, 51 Campus Dr., Saskatoon, Saskatchewan, Canada S7N5A8

* Corresponding author (rosalind.ball{at}usask.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The metabolic products of nitrogen fixation (N2) in a legume can be either amides (asparagine, glutamine) or ureides (allantoin and allantoic acid), which are then exported to the shoot via the xylem. Ureides are synthesized solely in the nodules. Chickpea (Cicer arientinum L.) has been separately classified as an amide and as a ureide exporter; however, the exact shoot metabolic products resulting from N2 fixation are not known. The objectives of this study were (i) to determine the metabolites of N2 fixation, namely free amino acids and ureides and (ii) to quantify the differences in N2 fixation for chickpea cultivars in the field by 15N natural abundance. Leaf ureide concentrations were analyzed at Weeks 6, 7, 8, 9, 10, and 11 after emergence. Free amino acid concentrations were analyzed at Weeks 7, 9, and 11 after emergence. Flax (Linum usitatissimum L., CDC-Bethune) was used as the reference crop for assessment of percentage nitrogen derived from the atmosphere. Two chickpea cultivars, CDC-Anna and Myles, had significantly higher N2 fixation than the other three tested cultivars. Myles also maintained ureides and amides at a moderate concentration from flowering through reproductive growth. Overall, we found that asparagine and alanine were the major free amino acids, along with ureides, representing likely metabolites from N2 fixation. Therefore, chickpea should be classified as both an amide and ureide exporter, on the basis of the concentration of both types of N product found in the shoot.

Abbreviations: Ec, electrical conductivity • %Ndfa, percentage nitrogen derived from the atmosphere • SPG, Saskatchewan Pulse Growers


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
LEGUME CROPS are economically important in cropping systems because of their ability to assimilate atmospheric nitrogen (N2). Biological N2 fixation occurs inside the root nodules of legume species as a result of a symbiosis between the host plant and bacteria. The metabolic products of N2 fixation in legumes are reported to be the amide asparagine or the ureides allantoin and allantoic acid (Streeter, 1991). Legumes transport N2 fixation products to the shoot via the xylem as ureides (Sinclair and Serraj, 1995), or mainly as asparagine and glutamine, with low concentrations of aspartic acid and homoserine (Peoples et al., 1987).

Chickpea appears to be a warm-season crop or at least intermediate between warm and cool-season legumes on the basis of its N2 fixation products. An earlier report suggested that chickpea exports ureides as the main N compound resulting from N2 fixation, but the exact concentrations were not reported (Pate and Atkins, 1983). Later, amides were suggested to be the main nitrogenous compounds translocated out of chickpea nodules, with asparagine in the range of 40 to 70% of nodule xylem N and glutamine in the range of 5 to 45% nodule xylem N (Peoples et al., 1987). Further, ureides were not measured in their study.

Recent studies in soybean [Glycine max (L.) Merr.], a warm-season legume, implied that control of N2 fixation during water deficit is mediated via cycling of metabolic products from the N2 fixation process (Bacanamwo and Harper, 1997; Purcell et al., 2000). Sinclair and Serraj (1995) reported that warm-season species that accumulated high concentrations of ureides (>200 mmol L–1 xylem sap) were more drought-sensitive than species with <50 mmol L–1 xylem sap or no ureide. However, no comparable measurements of asparagine or glutamine have been taken. Previously, Serraj and Sinclair (1997) recorded ureides and total amino acids in xylem sap of eight soybean cultivars including Biloxi and Jackson, and the drought tolerant cultivars had the lowest concentration of ureides in the xylem and in petioles. In the soybean cultivars Biloxi and Jackson, the main xylem-transported amino acids were asparagine, glutamine, {gamma}-aminobutyric acid, and proline, but ureides were not measured (Serraj et al., 1998).

Past studies have suggested chickpea may be an amide transporting legume because chickpea is a cool season crop (Pate and Atkins, 1983). However, a recent study showed that ureide metabolism was also involved, because urea was found to be a product of ureidoglycolate degradation in different organs of chickpea (Munoz et al., 2001). In this study, the authors did not directly assay the enzyme step of ureide catabolism, which produces the urea.

To date, no conclusive studies have been performed in chickpea to determine the metabolic products of N2 fixation in well-watered conditions or in drought, even though some research groups report amides and others report ureides. It is also not known if there are genotypic differences among chickpea cultivars in N metabolites and N2 fixation under well-watered conditions. The objectives of our study were to determine the metabolites of N2 fixation, namely free amino acids and ureides, in chickpea and to quantify the differences in N2 fixation by 15N natural abundance among chickpea cultivars in the field under well-watered conditions.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Field experiments were conducted in Saskatchewan, Canada, at one location in 2002 and two locations in 2003. The locations were Saskatoon (2002), Goodale (2003) and Saskatchewan Pulse Growers Land (SPG, 2003), and all locations were within a 30-km radius of Saskatoon, SK (52°09' N, 106°36' W). Soils at each location were Dark Brown Chernozems. Spring soil test values, average monthly precipitation and mean temperature during the summer at Saskatoon, 2002, and Kernen Farm Research Station, 2003 (within 15 km radius of Goodale and SPG locations) are presented in Table 1.


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  		Table 1. Soil physicochemical properties, precipitation, and mean temperature for the 2002 and 2003 growing seasons at three locations near Saskatoon, SK.

 
Cultivars Amit, CDC-Anna, CDC-Chico, CDC-Nika, and Myles were seeded in the field. These five chickpea cultivars were chosen on the basis of early maturity, leaf type (fern leaf), disease resistance, and high yield. Currently, these chickpea cultivars are best adapted to Dark Brown and Brown soils in Saskatchewan, Canada. Myles is widely grown in the northern USA, and the other cultivars have increasing production areas in North America. They were also the best five cultivars among eight previously tested in a growth chamber experiment, where selection was based on nodulation and their plant N requirement. The five cultivars and a reference crop were grown in each location in 2002 and 2003. Flax cv. CDC-Bethune was used as the non-fixing reference crop for the assessment of percentage N derived from the atmosphere (%Ndfa). Bremer and van Kessel (1990) suggested that the reference crop should have a similar rooting pattern and soil N uptake to the N2 fixing plant. Flax, like chickpea, has a short tap root system with fibrous branches. Rooting depth for both crops extended to a depth of over 1m depending on soil type. Plot size was 1.2 x 6.7 m with 0.3 m within and between row spacing. Commercial rhizobium inoculant was applied at the recommended rate (MicroBio RhizoGen Corp. Saskatoon, SK). Triple superphosphate (0–45–0) at the rate of 20 kg ha–1 P2O5 was applied at seeding; no nitrogen fertilizer was applied. The residual N was less than 32 kg ha–1 (Table 1). At each location, seeding was done by mid May and crops were grown until late vegetative stage before leaf sampling. The frost-free growing season at the sites was between 100 and 110 d. At Week 6 most of the cultivars at each location were in late vegetative growth and had begun to flower.

Tissue Analysis
Six of the uppermost fully expanded leaves were chosen at random from the two center rows of each plot at each location at 6, 7, 8, 9, 10, and 11 wk after emergence. Final leaf tissue samples were taken at the end of August for each location and year. Leaflets were separated from the petiole, oven-dried (40°C for 2 d), finely ground, and analyzed for ureide concentration. Free amino acid concentrations in those sampled leaves were analyzed only at the Saskatoon location at 7, 9, and 11 wk after emergence. Biomass was removed from 1 m2 of each plot at 6, 8, 10, and 12 wk after emergence for each location and biomass was oven-dried and finely ground. A sample of ground plant material was taken and analyzed for whole plant N content by combustion (LECO CNS 2000, St. Joseph, MI, USA). Plant N content was calculated by:

[1]

A 1-m2 area of chickpea or reference crop at maturity was hand-harvested from each plot, dried, ball-milled, and analyzed for isotopic composition by the method described in Stevenson and van Kessel (1997) on a 20–20 Mass Spectrometer interfaced with an ANCA-GSL sample converter (Europa Scientific, Crewe, UK). Shoot materials were sampled at ground level. Any dropped leaves and the root system were not included in the sample. The proportion of N derived from the atmosphere via biological nitrogen fixation (%Ndfa) in chickpea shoot was calculated as reported by Rennie and Kemp (1984):

[2]
where {delta}15N is:

{crop2497-eqn3}

The value for C represents the {delta}15N value of chickpea grown in an N-free medium in a growth chamber under following conditions: 22°C during the day and 20°C during the night. The C value for the shoot of chickpea plants was 1.009. The atom percentage of 15N of the atmosphere was 0.3663%, which was equal to a {delta}15N value of 0 (Mariotto, 1983). The amount of N fixed by each genotype was calculated by:

[4]
Seed yield was determined with a small plot combine for each location in early October.

A 30- to 35-mg sample of dry ground leaf sample from each plot was used to determine shoot ureide concentration using a modified colorimetric procedure (de Silva et al., 1996). Between 75 and 100 mg of homogenized oven dry leaf sample from each plot was used to extract free amino acids on the basis of a modified method of Leon-Guzman et al. (1997). One milliliter of CH3OH:CHCl3:H2O (12:5:3) solution was added to 100 mg of leaf sample and shaken for 16 h on a reciprocating shaker. Then the mixture was centrifuged at 10000 g for 5 min. A 100-µL aliquot of leaf extract was used to elute the free amino acids with the EZ: faast sample test kit (EZ: faast Phenomenex, Torrance, CA, USA). Free amino acids were analyzed on a gas chromatograph (6890 Series Gas Chromatograph Technologies, Agilent System, Wilmington, DE, USA) using a Zebron ZB-PAAC column (Phenomenex, Torrance, CA, USA). The EZ:faast method was developed for analysis of 40 aliphatic and aromatic amino acids (EZ: faast Phenomenex, Torrance, CA, USA). Mixtures of amino acid standards (20 nmol/100 µL) were used for every 10 injections to quantify amino acid concentration. Norvaline was used as the internal standard and quantifications were performed by comparing sample peak areas to the standard's peak areas.

Experimental Design and Statistical Analysis
The experimental design was a randomized complete block design with four replicates, at three location-years. Sampling for the variables ureide concentration, amino acid concentration, and whole plant nitrogen content were taken from random samples within plots over time. Data were analyzed separately for each location-year. Ureide concentration, amino acid concentration, and whole plant nitrogen content were analyzed for each sampling time separately. Analysis of variance was done by the General Linear Model procedure (PROC GLM) of SAS version 8.2 (SAS Institute, 1999). Means were separated by Fisher's protected LSD at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Soil Properties and Weather Data
The spring nutrient availability and weather data for each location are presented in Table 1. The soils of each location were clay loam. The pH ranged from 7.2 to 7.8 at 0- to 30-cm depth and no evidence of salinity was found. Spring available inorganic N concentration ranged from 22 to 32 kg ha–1 in the 0- to 30-cm depth and the amount was higher in SPG location compared with Saskatoon and Goodale. Extractable P was low while extractable K was relatively high. About 30 to 40 g kg–1 organic matter content was observed for each location in the 0- to 30-cm depth (Table 1). The Saskatoon location had above average precipitation from July to September, while Kernen had above average precipitation during April and July (Table 1). Generally, Goodale and SPG locations experienced dry conditions during summer compared with Saskatoon. The Saskatoon location had warm temperatures during June and July (2002), and the Kernen location had warm August temperatures in 2003.

Leaf Ureide Concentrations
Leaf ureide concentrations at Weeks 6 and 7 were low for all chickpea cultivars and ranged between 0.5 to 5 µmol g–1 (Table 2). Amit had a significantly higher ureide concentration compared with CDC-Chico at Week 6. Although Myles had a significantly higher leaf ureide concentration compared with CDC-Chico at Week 8, there were no significant differences among chickpea cultivars at Week 7. Myles showed significantly lower leaf ureide concentrations at Weeks 9, 10, and 11 compared with CDC-Chico. Cultivars were at late vegetative growth at Week 6 and flowering began at Week 8. There was a large increase in leaf ureide concentration of CDC-Chico after flowering. Furthermore, the amount of N2 fixation by CDC-Chico was low compared with the other cultivars.


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  		Table 2. Leaf ureide concentration (µmol g–1 dry leaf tissue) for field-grown chickpea cultivars.

 
Mean Leaf Free Amino Acid Concentration
Alanine, asparagine, and glutamic acid were the major N2 products resulting from N2 fixation of chickpea and their concentrations were >70 µmol g–1 leaf dry weight (Table 3). Methionine, proline, serine, threonine, and valine were the second major N2 products resulting from N2 fixation. The remaining free amino acids were at concentrations <10 µmol g–1 of dry leaf tissue.


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  		Table 3. Mean leaf free amino acid concentration during reproductive growth, averaged over five chickpea cultivars grown in the field, Saskatoon, 2002.

 
Alanine and asparagine concentrations over the sampling times were variable and differed depending on cultivar (Fig. 1) . Alanine concentrations ranged between 135 µmol g–1 for CDC-Nika on Week 9 and 561 µmol g–1 for CDC-Nika on Week 11 when observing the variation across all cultivars from Weeks 7, 9, and 11. Asparagine concentrations ranged between 148 µmol g–1 for CDC-Nika on Week 9 and 333 µmol g–1 for Myles on Week 11 when observing the variation across all cultivars from Weeks 7, 9, and 11. Both alanine and asparagine concentrations decreased between Weeks 7 and 9 and then increased by Week 11 for an unknown reason (Table 3). Glutamic acid concentration increased at Week 9 to 121 µmol g–1 and then decreased at Week 11 to 79 µmol g–1 (Table 3). Methionine, proline, threonine, and valine increased over the sampling time but serine increased only at Week 9 to 35 µmol g–1 before decreasing to 31 µmol g–1 at Week 11 (Table 3). Aspartic acid, glutamine, histidine, isoleucine, leucine, lysine, and tryptophan increased over the sampling time (Table 3).



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  		Fig. 1. Alanine, asparagine, and glutamic acid concentration after flowering for field grown chickpea cultivars at Saskatoon, 2002. Comparisons made each week separately. Within a week, different letters above bars indicate that means for specific amino acids among the cultivars were significantly different at P < 0.05.

 
Overall, these results indicate that free amino acids are the major nitrogen metabolites compared with ureides. Most of the amino acids concentrations tended to increase at Week 11 except glutamic acid and glycine (Table 3). Most genotypic differences in free amino acid concentrations found in the leaves were observed at Week 9, which corresponded to late flowering and early pod formation.

Leaf Free Amino Acid Concentration Differences among the Cultivars
Cultivar differences in some free amino acids were observed at Weeks 9 and 11 (Fig. 1). At Week 7, no cultivar differences were observed except for isoleucine and serine (data not shown). Most cultivar differences in free amino acid concentrations in chickpea were observed at Week 9 (Fig. 1). CDC-Chico had a significantly higher alanine concentration compared with CDC-Nika at Week 9. Amit had a significantly higher asparagine concentration compared with CDC-Nika. Although CDC-Nika had lower alanine and asparagine concentrations at Week 9, its glutamic acid concentration was significantly higher compared with the other cultivars. CDC-Chico had a significantly lower asparagine concentration and a significantly higher glutamic acid concentration compared with Myles at Week 11.

Asparagine and alanine concentrations were higher in Myles at the beginning and at the end of the sampling period (Fig. 1). This may be due to Myles having an ability to maintain N2 fixation products at a medium level throughout the growing season. However, Myles did have a significantly lower asparagine concentration compared with Amit at Week 9, indicating more N demand after flowering. Similarly, Myles had significantly lower concentrations of other amino acids such as glycine, lysine, phenylalanine, serine, and tryptophan at Week 9 compared with the other cultivars. The role of these amino acids in the metabolism of N2 fixation products during drought is not yet known.

Whole Plant N Content, Seed Yield, and Percentage N Derived from Atmosphere
As anticipated, whole plant N content increased for all chickpea cultivars over the growing season; however, a significant cultivar effect was observed only at Weeks 6 and 10 (Table 4). At Week 6, CDC-Nika had a significantly higher plant N content compared with CDC-Anna and Myles. Amit had a significantly higher plant N content compared with Myles at Week 10. Seed yield of CDC-Anna from the three sites was significantly lower than the other chickpea cultivars (Table 4). Seed yield for CDC-Anna in 2002 was low at Saskatoon because of frequent rain, flood, and disease. The seed yield average over two locations in 2003 for CDC-Anna ranged between 1100 and 1500 kg ha–1, which was similar to the other chickpea cultivars. Although CDC-Anna had lower seed yield, %Ndfa was significantly higher than CDC-Chico and Amit. Myles, CDC-Nika and CDC-Anna were the highest N2 fixing cultivars and CDC-Chico was the lowest. Myles did not have a significantly lower total N content, meaning that the moderate concentrations of ureides are not a result of lower N2 fixation but likely a continued and steady metabolism.


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  		Table 4. Whole plant N, grain yield, percentage N derived from the atmosphere, and amount of N2 fixation for field-grown chickpea cultivars.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Asparagine and alanine were the major shoot free amino acids found, implying these are candidates for metabolic products resulting from N fixation, but chickpea also produced ureides that accumulated in leaves to between 0.5 to 3.8 µmol g–1 dry weight. This is the first study reporting chickpea cultivar variation in free amino acids associated with N2 fixation under field conditions and that chickpea also has a high concentration of alanine (up to 560 µmol g–1).

Chickpea has N2 metabolism that is comparable with the ureide exporting legumes soybean and cowpea (Hong and Copeland, 1990), so ureides would be expected as metabolic products. Similar to the Hong and Copeland (1990) study, Munoz et al. (2001) found catabolic ureide enzyme activities. They reported that the presence of the ureidoglycine aminohydrolase enzyme complex increased the production of ureidoglycolate in chickpea leaves. The presence of ureidoglycolate urea-lyase or ureidoglycine aminohydrolase further breaks ureidoglycolate into glyoxylate. The presence of ureidoglycolate urea-lyase activity demonstrates the existence of a urea-producing pathway for ureide catabolism in chickpea. This means chickpea has an ability to produce ureides as metabolites resulting from N2 fixation. Results from Hong and Copeland (1990) and Munoz et al. (2001) fit our experimental results in that both asparagine and ureides can be major shoot metabolites resulting from N2 fixation in chickpea. However, from our data, asparagine is the free amino acid found at the highest concentration, 213 to 290 µmol g–1 of dry leaf tissue (with a ratio of 2 moles N for every mole of asparagine), and allantoin and allantoic acid are at lower concentrations, with about 1 to 4 µmol g–1 of dry leaf tissue (with a ratio of 4 moles N for every mole of ureide). We found chickpea cultivars maintained ureide concentrations during the growing season, but poor N2 fixing chickpea cultivars showed high ureides and low asparagine concentrations at the end of the growing season.

Under field conditions in Syria, Beck (1992) reported %Ndfa value for chickpea ranged from 0 to 80% and the average value for N2 fixation ranged from 19 to 24 kg N ha–1 during a dry year. Carranca et al. (1999) reported %Ndfa in developing pods of chickpea ranged from 30 to 80% under field conditions with or without inoculants. Although, %Ndfa values from the straw and pod of chickpea were similar, Carranca et al. (1999) suggested that chickpea remobilized large amounts of N from vegetative parts to pods during reproductive stage. Typically under dryland conditions shoot N derived from N2 fixation in chickpea represents to 40 kg N ha–1 and this amount of N2 fixation appears to be similar or marginally higher under irrigated conditions (Unkovich and Pate, 2000). Values of %Ndfa and N2 fixed by chickpea in our experiment were similar to the results reported by Beck (1992) and Carranca et al. (1999). Amit and CDC-Chico had lower %Ndfa values compared with Myles. Myles and CDC Chico represented the range of nitrogen fixation (10–50%) seen in cultivars grown in western Canada. Possible reasons for low %Ndfa in Amit and CDC-Chico were the high ureide and glutamic acid concentrations, coupled with a low asparagine concentration at the end of the growing season. A labeling study has shown that accumulation of asparagine and ureides increases the pool of soluble N in faba bean (Vicia faba L.) that can cause a feedback inhibition effect on the nitrogenase activity (Oti-Boateng and Silsbury, 1993). CDC-Chico has an indeterminate growth habit and grows to a large size with many branches, and shows N deficiencies after flowering in both the field and growth chamber. Late season symptoms of N deficiency in such cultivars are consistent with a high ureide concentration after flowering, which may cause a feedback effect on N2 fixation and which subsequently reduces asparagine concentration.

The cultivar Myles maintained ureides and amides at a moderate concentration for a longer time compared with the other tested chickpea cultivars in the field. Asparagine was the principle export product that was accumulated in young pea leaves under drought conditions (Ta et al., 1985). Asparagine synthesis occurs via a glutamine-dependent amidation of aspartate. Active transport mechanisms may contribute to low amino acid concentration in nodules. Active transport of amino acids can then create a greater diffusion gradient between symbiosome and cytosol that may cause a feed back inhibition on the nitrogenase activity (Ta et al., 1985).


   ACKNOWLEDGMENTS
 
This research was funded by NSERC and Saskatchewan Pulse Growers Association in Canada.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 




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