Journal of Experimental Botany, Vol. 52, No. 359, pp. 1209-1217,
June 1, 2001
© 2001 Oxford University Press
Original Papers |
Mapping of QTLs associated with cytosolic glutamine synthetase and NADH-glutamate synthase in rice (Oryza sativa L.)
1 Department of Applied Plant Science, Graduate School of Agricultural Sciences, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan
2 Plant Breeding, Genetics and Biochemistry Division, International Rice Research Institute, MCPO BOX 3127,1271 Makati City, Philippines
3 Department of Molecular Genetics, National Institute of Agrobiological Resources, 2-1-2 Kannondai, Tsukuba 305-8602, Japan
4 Department of Cell Biology, National Institute for Basic Biology, Okazaki 444-8585, Japan
5 Plant Science Center, RIKEN, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
6 Graduate School of Life Science, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai 980-8577, Japan
Received 6 October 2000; Accepted 13 February 2001
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Abstract |
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Ninety-eight backcross inbred lines (BC1F6) developed between Nipponbare, a japonica rice, and Kasalath, an indica rice were employed to detect putative quantitative trait loci (QTLs) associated with the contents of cytosolic glutamine synthetase (GS1; EC 6.3.1.2) and NADH-glutamate synthase (NADH-GOGAT; EC 1.4.1.14) in leaves. Immunoblotting analyses showed transgressive segregations toward lower or greater contents of these enzyme proteins in these backcross inbred lines. Seven chromosomal QTL regions for GS1 protein content and six for NADH-GOGAT protein content were detected. Some of these QTLs were located in QTL regions for various biochemical and physiological traits affected by nitrogen recycling. These findings suggested that the variation in GS1 and NADH-GOGAT protein contents in this population is related to the changes in the rate of nitrogen recycling from senescing organs to developing organs, leading to changes in these physiological traits. Furthermore, a structural gene for GS1 was mapped between two RFLP markers, C560 and C1408, on chromosome 2 and co-located in the QTL region for one-spikelet weight. A QTL region for NADH-GOGAT protein content was detected at the position mapped for the NADH-GOGAT structural gene on chromosome 1. A QTL region for soluble protein content in developing leaves was also detected in this region. Although fine mapping is required to identify individual genes in the future, QTL analysis could be a useful post-genomic tool to study the gene functions for regulation of nitrogen recycling in rice.
Key words: Cytosolic glutamine synthetase, NADH-glutamate synthase, nitrogen recycling, QTL, rice (Oryza sativa L.).
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Glutamine synthetase (GS; EC 6.3.1.2) is the key enzyme involved in the assimilation of ammonia in plants. GS catalyses the ATP-dependent condensation of NH3 with glutamate to produce glutamine. Subsequently, glutamate synthase (GOGAT) catalyses the reductive transfer of the amide group of glutamine to 2-oxoglutarate to form two glutamate molecules (Ireland and Lea, 1999
). In Sasanishiki, a leading cultivar of Japanese lowland rice (Oryza sativa L.) in northern Japan, c. 80% of total nitrogen in the panicle is remobilized through the phloem from older, senescing organs (Mae and Ohira, 1981). Therefore, the process of nitrogen recycling is very important in determining both the productivity and quality of rice. Glutamate is a major free amino acid in the leaf blades (Kamachi et al., 1991), whereas glutamine and asparagine, which is synthesized from glutamine (Lea et al., 1990; Sechley et al., 1992; Ireland and Lea, 1999), are major forms of the total amino acids in phloem sap of rice plants (Hayashi and Chino, 1990). Therefore, conversion of glutamate to glutamine is required during the process for remobilization of leaf nitrogen from the senescing leaves. Also, the synthesis of glutamate from glutamine that is transported through the vascular system from the senescing tissues, as well as from roots, is required to support further biosynthetic processes which occur in the young developing tissues. Cytosolic glutamine synthetase (GS1) is important for the export of nitrogen from senescing leaves, because the GS1 protein was detected in companion cells, which are important for the phloem loading of solutes, and vascular parenchyma cells (Sakurai et al., 1996; Obara et al., 2000). NADH-dependent glutamate synthase (NADH-GOGAT; EC 1.4.1.14) in developing organs, such as unexpanded non-green leaves and developing grains, could be involved in the utilization of remobilized nitrogen, because NADH-GOGAT protein is located in the specific cell types which are important for solute transport from the phloem and xylem elements (Hayakawa et al., 1994).
Recent progress of genetic manipulation will probably permit external alterations in the rate of nitrogen recycling. For example, over-expression or antisense inhibition of target genes, such as GS1 and NADH-GOGAT in the present case, could alter the phenotypic properties for the rate of nitrogen recycling, plant growth and yield (Yamaya et al., 2000). Another approach for improving nitrogen recycling could be the use of genetic resources of rice plants. Oryza sativa, a cultivated rice crop native in Asia, has genetic diversity and is classified into three types or subspecies, i.e. japonica, indica and javanica (Takahashi, 1984). Previously, it was shown that more than half of the indica cultivars examined had a 2-fold higher GS1 protein content in the senescing leaf blade than most japonica cultivars on a leaf fresh weight basis (Yamaya et al., 1997; Obara et al., 2000). On the other hand, the NADH-GOGAT protein content in the unexpanded young leaf blade was significantly lower in most indica cultivars than in japonica cultivars (Yamaya et al., 1997; Obara et al., 2000).
Plant phenotype, including the content of target enzyme protein, is determined by a number of gene activities, as well as agronomic and physiological traits (Goldman et al., 1993). Molecular cloning of all genes is one way to understand phenotypic characteristics. This upward method is, however, not easy to cover all genes, because the individual effect of each gene on the phenotype could be relatively small. Alternatively, DNA markers and their linkage map on chromosomes are efficient tools and methods for mapping individual QTLs (Tanksley, 1993; Paterson, 1995), as well as the recent progress of DNA array and proteome analyses as post-genomics tools in Arabidopsis and green algae. A number of QTL analyses using interspecific crosses have been conducted to identify the loci controlling physiological traits in various crop plants. In rice, QTL analysis with DNA markers, based on a well-saturated genetic linkage map, has been employed to detect genomic regions associated with several traits exhibiting complex inheritance (Yano and Sasaki, 1997). As far as is known, however, there have been no trials to combine genetic traits of rice and biochemical/molecular biological characteristics in QTL analysis. Such downward analyses could provide valuable information on many genes related to the regulation of target steps for specific traits.
As the first step to identify many genes related to nitrogen recycling, the locus of GS1 was mapped and the QTLs associated with GS1 protein content in the senescing leaf blade and NADH-GOGAT protein content in the developing leaf blade were detected. The physiological and agronomic traits that overlapped with these QTLs for GS1 and NADH-GOGAT protein content are discussed.
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Materials and methods |
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Plant materials
Ninety-eight backcross inbred lines (BILs; BC1F6) developed from advanced backcross lines (BC1F1; Nipponbare/Kasalath//Nipponbare) for six generations by the single seed descent method were used in this study. The japonica rice Nipponbare (Japanese lowland rice) is a leading cultivar in south-east Japan, whereas indica rice Kasalath originated from Assam, India.
The seeds of BILs (BC1F6) and their parents were imbibed in distilled water at 30 °C for 2 d. Germinated seeds were sown on a synthetic culture soil (Mitsui-Toatsu No. 3, Tokyo, Japan) in a small container (diameter 1.5x3 cm). Twenty days later, three seedlings of each line or parent were then transplanted per 4.0 l plastic pot (diameter 18x20 cm) with 3 kg of soil supplement (pH 4.5–5.0, less than 3.5 mm in particle size) with 3.0 g of slow-release fertilizer (N, 16%; P2O5, 16%; K2O, 16%: Coop Chemical Co. Ltd, Tokyo, Japan) in a glasshouse with irrigation.
Mapping of the GS1 locus
The GS1 specific fragment for 98 BILs and their parents was amplified by PCR using primers based on a sequence of GS1 genomic clone for Sasanishiki (Kojima et al., 2000). Sequences of the forward and reverse primers for PCR were 5'-AGATCATCAAGTCCGCCATT-3' and 5'-TGGTAGCATGCAACCAAATC-3', respectively. These amplified fragments were digested with HhaI, and then separated by electrophoresis on a 3.5% acrylamide gel (Goto et al., 1998). GS1 was mapped using MAPMAKER/EXP (Lander et al., 1987) as described previously (Lin et al., 1998).
Quantification of GS1 and NADH-GOGAT proteins by immunoblotting
When the 11th leaf blade from the base of the main stem of each plant was just emerged from the 10th leaf sheath, the ninth leaf blade was harvested for assay of GS1 protein. The non-green portion of the 11th leaf blade was used for assay of NADH-GOGAT protein. Fresh leaves were weighed, frozen in liquid nitrogen, and stored at -80 °C until required. Two independent samples at all leaf positions of each line and their parents were provided for each experiment. The frozen leaf samples were homogenized with a mortar and pestle in the presence of washed sand in extraction buffer as described previously (Yamaya et al., 1995). The crude protein fraction was prepared from the homogenate, separated by SDS-PAGE, and immunoblotted with the corresponding affinity-purified IgG as described previously (Yamaya et al., 1992). The immunoreacted GS1 and NADH-GOGAT polypeptides were visualized and quantified densitometrically (Hayakawa et al., 1993). The soluble protein content was determined by the methods using bovine serum albumin as the standard (Bradford, 1976).
Evaluation of physiological traits
Plants of the BILs and their parents were grown to maturity in a glasshouse for evaluating the leaf senescence and the physiological traits, i.e. spikelet number per panicle on the main stem (SPN), panicle weight on the main stem (PNW), and one-spikelet weight (SPW). Chlorophyll content of flag leaves at the 5 cm-tip region was measured by a SPAD-meter 502 (Minolta Co. Ltd, Tokyo, Japan) every 7 d for 5 weeks from flowering to maturity. Rates for half-discoloration (RHD) and full-discoloration (RFD) of leaf chlorophyll were determined using the following equation.
 | (001) |
At 50 d after flowering, the panicle on the main stem was harvested and dried for 2 weeks in a well-ventilated room with an electric-fan. Then, the spikelet number per panicle and panicle weights on the main stem were measured. One-spikelet weight was determined as the mean value of ten superior spikelets (well-filled).
Molecular markers and QTL detection
The molecular marker data for the BILs were essentially the same as those described earlier (Lin et al., 1998), which consisted of 245 restriction fragment length polymorphisms (RFLP) covering all 12 chromosomes. This data set was used for mapping the BIL putative genes for the quantitative traits. Single-marker regressions were used to detect the association between markers and each trait using a computer program qGENE (Nelson, 1997). Significant (P<0.05) differences in marker class means were interpreted as likely linkage of each trait to the marker locus. The percentage of the total phenotypic variation explained by QTLs identified for each trait was estimated as the R2 value. Multiple regression analysis was employed to detect the effects of two QTLs on the total phenotypic variation for the content of GS1 and NADH-GOGAT proteins in leaf blades. The log-likelihood (LOD) score in qGENE indicates the strength of the data supporting the hypotheses about the existence of the QTL for physiological traits. QTL positions were assigned at the point of maximum LOD score (i.e. the QTL peak) in the regions under consideration. Two QTL positions on the same chromosome were regarded as different when the distance of nearest markers of each QTL was more than 10 cm.
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Results |
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Variation in biochemical traits
The GS1 protein content based on leaf fresh weight in the BILs was in between that of Kasalath (9.70 µg g-1 FW) and Nipponbare (6.47 µg g-1 FW), although the mean value was closer to Nipponbare (Fig. 1A
). The GS1 protein content in the BILs showed a continuous distribution with one peak ranging from 2.55 to 16.18 µg g-1 FW, and demonstrated transgressive segregation in both directions. In BILs, the GS1 protein content was approximately 6 times higher in the highest BIL than in the lowest BIL.
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On the other hand, the NADH-GOGAT protein content in the developing leaf blade of Kasalath and Nipponbare was 2.16 and 3.08 µg g-1 FW, respectively (Fig. 1B
). Also, the NADH-GOGAT protein content in BILs was continuously distributed with one peak ranging from 1.27 to 4.48 µg g-1 FW, the mean value of the BILs being within the range of the parents.
The soluble protein content in senescing leaf blades of Kasalath and Nipponbare was 24.8 and 33.1 mg g-1 FW, respectively (Fig. 1C). The soluble protein content in BILs ranged from 14.6 to 44.2 mg g-1 FW with a mean of 26.9 mg g-1 FW. In the developing leaf blade, the soluble protein content of Kasalath was nearly the same as that of Nipponbare (Fig. 1D). However, in BILs it showed a continuous distribution with one peak ranging from 8.5 to 20.2 mg g-1 FW, and the mean value was greater than that of the parents. This distribution appeared also to show transgressive segregation, because some BILs lay outside the range of the two parents. Therefore, these biochemical traits (the contents of GS1, NADH-GOGAT, and soluble protein) in rice plants are considered to be quantitative traits.
Variation in physiological traits
The mean value of SPN in Kasalath was 145 per panicle on the main stem, 130% higher than that in Nipponbare (Fig. 2A). Furthermore, the mean value of PNW in Kasalath was 2.63 g, 81% higher than that in Nipponbare (Fig. 2B). On the contrary, the SPW in Kasalath was 18.0 mg, 33% lower than that in Nipponbare (Fig. 2C). These physiological traits of BILs showed a continuous distribution from 33 to 162 for SPN, from 0.41 to 2.54 g for PNW, and from 16.9 to 30.1 mg for SPW.
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The rate for half-discolouring (days from heading to half-discoloration in the flag leaf=RHD) and that for full-discolouring (days from heading to full-discoloration in the flag leaf=RFD) in Kasalath were 34 d, 25 d shorter than those in Nipponbare, respectively (Fig. 2C
, D). RHD and RFD in the BILs ranged continuously from 19.6 to 51.2 d and from 23.6 to 79.2 d, respectively. All physiological traits appeared to show transgressive segregation, because in some BILs the mean values were always outside the range of the two parents. Therefore, these physiological traits were inherited in a quantitative fashion, as were the biochemical traits described above.
Mapping of the GS1 locus
The GS1 gene was mapped between C560 and C1408 in chromosome 2 (Figs 3, 4). The genetic distance was 10.8 cM from C560 and 0.8 cM from C1408, where the GS1 gene was detected to overlap with a putative QTL for SPW. However, there was no putative QTL for both RHD and RFD in the region where the GS1 gene locus was mapped on chromosome 2.
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QTLs for GS1 protein content
Based on the single-marker analysis, a total of seven putative QTLs (P<0.05) associated with GS1 protein content in senescing leaf blades were detected in the BILs (Table 1). These putative QTLs were located in the vicinity of R1826 and C777 on chromosome 2, C107 on chromosome 4, R1943 on chromosome 8, and C950, S2260 and R728 on chromosome 11. As indicated in Table 1, the LOD score for all putative QTLs for GS1 protein content was more than 0.9 unit. The percentage of phenotypic variation explained by each putative QTL for GS1 protein content was in the range from 4.4% to 6.3% and that explained by multiple QTLs was 21.8%.
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Five of the seven putative QTLs identified for GS1 protein content overlapped on a part of the QTL region for biochemical and/or physiological traits (Figs 3
, 4). A QTL linked to the marker C777 on chromosome 2 was located on the QTL regions for soluble protein content in the senescing leaf and developing leaf. Two QTL regions for GS1 protein content on chromosome 2 overlapped with the QTL regions for SPN and PNW. In this case, the alleles from Kasalath contributed to increases in GS1 protein content, while the alleles negatively contributed to SPN and PNW. One QTL (linked marker C950) for GS1 protein content on chromosome 11 was located in the QTL regions for PNW, SPW and RFD. In this case, the allele from Nipponbare contributed to the increase in GS1 protein content and promoted the rate of discoloration in the flag leaf. Other QTLs for GS1 protein content linked to marker R728 on chromosome 11 were located close to the QTL regions for SPW and the rate of discoloration in the flag leaf (RHD and RFD). In this case, the alleles from Kasalath contributed to the increase in GS1 protein content and promoted the rate of discoloration in the flag leaf.
QTL for NADH-GOGAT protein content
A total of six putative QTLs associated with NADH-GOGAT protein content in the developing leaf blade were also detected using the single-marker analysis (Table 1). These putative QTLs were located in the vicinity of C122 and C808 on chromosome 1, C1221 and R712 on chromosome 2, R1783 on chromosome 4, and C261 on chromosome 7. The total phenotypic variation explained by these six putative QTLs was 19.4%. The percentage of phenotypic variation explained by each QTL ranged from 4.4% to 7.7%.
The QTL linked to the marker C122 was located close to the marker D16060 encoding the NADH-GOGAT structural gene on chromosome 1 (Sasaki et al., 1994). One QTL for NADH-GOGAT protein content on chromosome 1 was located in a QTL region for soluble protein content in developing leaves (Fig. 3). Furthermore, two of the six QTLs for NADH-GOGAT protein content were located in QTL regions for other physiological traits (Fig. 4). One QTL linked to the marker C1221 on chromosome 2 was located in QTL regions for SPN and SPW. In this case, the alleles from Kasalath contributed to increases in NADH-GOGAT protein content and SPN, while the alleles negatively contributed to SPW. Other major QTLs linked to the marker R712 on chromosome 2 were located in the vicinity of QTL regions for soluble protein content, SPN, RFD and RHD. In this case, the alleles from Nipponbare contributed to an increase in NADH-GOGAT protein content and promoted the rate of discoloration in the flag leaf, while the alleles negatively contributed to SPN.
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Discussion |
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Previously, it had been found that the indica type Kasalath possessed approximately a 2-fold greater content of GS1 protein in senescing leaf blades than japonica type Nipponbare (Obara et al., 2000
). However, Kasalath showed a significantly lower content of NADH-GOGAT protein in developing leaf blades. It is assumed that GS1 activity in senescing leaves and NADH-GOGAT activity in developing organs are the major factors in determining the velocity of nitrogen recycling. The first step for validation could be to analyse the correlation between trait values including enzyme contents and allelic polymorphism.
The indica cultivars are different in morphology compared with japonica cultivars, including plant height, size of leaf blade and grain, numbers of tillers, as well as their yield and biomass production (Takahashi, 1984). Even when grown in a temperate area (e.g. Sendai, Japan) under conditions different from their native habitat, most indica cultivars including Kasalath appeared to retain their characteristics for high productivity (Yamaya et al., 1997). Furthermore, leaf senescence is faster in indica cultivars than that in japonica cultivars (Yoshida, 1981). During leaf senescence, decline in photosynthetic activity, discoloration of leaves and remobilization of nitrogen from senescing leaves to developing organs occurred. Nitrogen recycling is thus important in determining the productivity and quality, because a large proportion of nitrogen in the panicle originates from senescing organs (Mae and Ohira, 1981).
In this study, seven chromosomal regions having QTLs associated with GS1 protein content in the senescing leaf blade and six with NADH-GOGAT protein content in the developing leaf blade were detected (Table 1). The choice of statistical threshold is particularly important in QTL analysis, because the number of detected QTLs would be different when using a different threshold for the analysis (Yano and Sasaki, 1997). A low threshold (P<0.05 in ANOVA) was used to avoid a false-negative result in this study. Three putative QTLs for GS1 including the major QTL (linked to the marker S2260) on chromosome 11 were detected in the vicinity of QTL regions for physiological traits (Fig. 4). Alleles from Nipponbare and Kasalath that were identified with a higher GS1 protein content were also associated with a higher rate of leaf discoloration in the case of QTLs linked with the markers C950 and R728, respectively (data not shown). Therefore, the alleles that increased the GS1 protein content promoted the rate of leaf senescence (RHD and RFD). These results suggest that variation of the GS1 protein content in this population might change the rate of export of Gln from senescing organs to developing organs and then lead to changes in these physiological traits.
Similarly, two putative QTLs for NADH-GOGAT content including a major one (linked to the marker R712) on chromosome 2 were detected in the vicinity of QTLs for SPN and PNW (Fig. 4). In the case of QTLs linked to the marker R712, the alleles from Nipponbare were associated with an increase of NADH-GOGAT protein content and a decrease of SPN. Furthermore, putative QTLs for NADH-GOGAT protein content on chromosome 1 were located in the QTL region for soluble protein content in developing leaves. At these QTLs, the alleles from Kasalath were identified with an increase of NADH-GOGAT protein content and soluble protein content in developing leaves. These findings suggested that the variation in NADH-GOGAT protein content in this population is related to changes in the rate of regeneration of Glu from Gln transported via the phloem and xylem in developing organs leading to changes in protein content.
Overexpression of GS1 in shoots accelerated plant development in transgenic Lotus cornculatus, leading to early senescence and premature flowering in plants grown on an ammonium-rich medium (Vincent et al., 1997). This is in agreement with the present finding that changes in the GS1 protein content in this BIL population affect leaf senescence (RHD and RFD). Analyses of transgenic rice plants expressing antisense RNA for NADH-GOGAT at the T3 generation showed significant decreases in PNW, SPW, and tiller number, but a significant increase in SPN (Ishiyama et al., unpublished results). These results also indicate that the variation in NADH-GOGAT protein content among BIL populations accounts for variation in SPN and SPW. Manipulation of a target gene is a powerful system to understand the function of the gene product, but it is difficult to identify other genes responsible for the regulation of the gene products. On the other hand, QTL analysis provides multiple independent loci which could be expected to have regulatory functions on the gene products, although fine mapping is needed to identify these genes. A combination of these two systems may be useful to elucidate the nitrogen recycling mechanism.
A locus of the structural gene coding for GS1 was mapped on chromosome 2 between C560 and C1408 (Figs 3, 4). This locus corresponded to the region established as a QTL for one-spikelet weight (Fig. 4). In maize, three of the five loci corresponding to GS structural genes were located on the region of QTLs for one thousand-kernel weight (Bertin et al., 1997). These findings suggested that GS1 enzyme in the leaf blade is an important factor for grain-filling in cereals. It was reported that a locus of the structural gene encoding NADH-GOGAT was mapped on chromosome 1 between C1370 and C122 (Sasaki et al., 1994) (Fig. 3). This structural gene was located in the region of a putative QTL associated with NADH-GOGAT protein content.
It was shown that QTLs for the activities of sucrose-phosphate-synthase and acid-soluble invertase were detected in the regions where each structural gene was mapped (Prioul et al., 1999). Furthermore, these QTLs were located close to QTLs for the contents of products and substrates of each enzyme. In these experiments, two out of seven QTLs for GS1 protein content and three out of six QTLs for NADH-GOGAT protein content were detected in different regions from other biological and physiological traits (Figs 3, 4). To identify the candidate genes from the QTL analysis more precisely, it is necessary to investigate lines near isogenic in the QTL region. Elucidation of the genetic nature regulating GS1 and NADH-GOGAT protein contents as a whole could aid in the efficient breeding of high-performance rice cultivars.
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Acknowledgments |
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We would like to thank Dr Shao Yang Lin for helpful comments on the manuscript. This work was supported in part by a programme of Research for the Future from the Japan Society for the Promotion of Science (JSPS-RFTF96L00604) and in part by Grants-in-Aid for Scientific Research (Nos 10556075 and 09NP0901) from the Ministry of Education, Science and Culture, Japan and CREST of JST (Japan Science and Technology).
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Notes |
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7 To whom correspondence should be addressed. Fax: +81 22 263 9845. E-mail: tadashi{at}ige.tohoku.ac.jp
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B. Hirel, J. Le Gouis, B. Ney, and A. Gallais The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches J. Exp. Bot., July 1, 2007; 58(9): 2369 - 2387. [Abstract] [Full Text] [PDF]
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 J. M. Cross, M. von Korff, T. Altmann, L. Bartzetko, R. Sulpice, Y. Gibon, N. Palacios, and M. Stitt Variation of Enzyme Activities and Metabolite Levels in 24 Arabidopsis Accessions Growing in Carbon-Limited Conditions Plant Physiology, December 1, 2006; 142(4): 1574 - 1588. [Abstract] [Full Text] [PDF]
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 T. Kichey, J. Le Gouis, B. Sangwan, B. Hirel, and F. Dubois Changes in the Cellular and Subcellular Localization of Glutamine Synthetase and Glutamate Dehydrogenase During Flag Leaf Senescence in Wheat (Triticum aestivum L.) Plant Cell Physiol., June 1, 2005; 46(6): 964 - 974. [Abstract] [Full Text] [PDF]
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L. Yang, S. Mickelson, D. See, T. K. Blake, and A. M. Fischer Genetic analysis of the function of major leaf proteases in barley (Hordeum vulgare L.) nitrogen remobilization J. Exp. Bot., December 1, 2004; 55(408): 2607 - 2616. [Abstract] [Full Text] [PDF]
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S. Mickelson, D. See, F. D. Meyer, J. P. Garner, C. R. Foster, T. K. Blake, and A. M. Fischer Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves J. Exp. Bot., February 1, 2003; 54(383): 801 - 812. [Abstract] [Full Text] [PDF]
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O. Loudet, S. Chaillou, P. Merigout, J. Talbotec, and F. Daniel-Vedele Quantitative Trait Loci Analysis of Nitrogen Use Efficiency in Arabidopsis Plant Physiology, January 1, 2003; 131(1): 345 - 358. [Abstract] [Full Text] [PDF]
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A. M. Limami, C. Rouillon, G. Glevarec, A. Gallais, and B. Hirel Genetic and Physiological Analysis of Germination Efficiency in Maize in Relation to Nitrogen Metabolism Reveals the Importance of Cytosolic Glutamine Synthetase Plant Physiology, December 1, 2002; 130(4): 1860 - 1870. [Abstract] [Full Text] [PDF]
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T. Yamaya, M. Obara, H. Nakajima, S. Sasaki, T. Hayakawa, and T. Sato Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice J. Exp. Bot., April 15, 2002; 53(370): 917 - 925. [Abstract] [Full Text] [PDF]
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B. J. Miflin and D. Z. Habash The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops J. Exp. Bot., April 15, 2002; 53(370): 979 - 987. [Abstract] [Full Text] [PDF]
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