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Published online 24 February 2006
Published in Crop Sci 46:763-773 (2006)
© 2006 Crop Science Society of America
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CROP PHYSIOLOGY & METABOLISM

Identification of Quantitative Trait Loci for {delta}13C and Productivity in Irrigated Lowland Rice

Ma. R. Lazaa, M. Kondoa,*, O. Idetaa, E. Barlaanb and T. Imbea

a Department of Rice Research, National Institute of Crop Science (NICS), 2-1-18, Kannondai, Tsukuba-city, Ibaraki, 305-8518, Japan
b Nagasaki Industrial Promotion Foundation, 5-717-1 Fukahori, Nagasaki-city, Nagasaki, 851-0301, Japan

* Corresponding author (chokai{at}naro.affrc.go.jp)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Stable carbon isotope ratio ({delta}13C) in plants has been suggested as a useful indicator for cumulative Ci/Ca signature in a leaf, water use efficiency, and crop productivity, and is known to have genotypic variation in rice (Oryza sativa L.). We conducted a field study to identify quantitative trait loci (QTLs) for {delta}13C and other related leaf traits, such as leaf N, specific leaf area, and SPAD value, using recombinant inbred lines derived from an indica x japonica cross grown under flooded conditions. We also examined the genetic associations of {delta}13C with yield, yield components, and biomass productivity. Putative QTLs for {delta}13C were identified on chromosomes 2, 4, 8, 9, 11, and 12 across plant parts, stages, and years. Differential expression of QTL for {delta}13C among stages suggests that each QTL had different functions by stages. The QTLs for {delta}13C were associated with a few colocated QTLs for leaf traits indicating that their physiological and genetic associations with leaf traits may be complex. Values of {delta}13C at maturity were negatively correlated with harvest index and grain yield. However, genetic association of these traits could not be clarified due to the absence of co-located QTLs. Further examination would be useful to elucidate the physiological and morphological functions of QTLs for {delta}13C found in this study.

Abbreviations: Ci/Ca, ratio of intercellular and ambient partial pressures of CO2 • CID, carbon isotope discrimination • {delta}13C, 13C/12C ratio expressed with a differential notation • DTH, days to heading • HI, harvest index • LOD, logarithm of the odds • NPT, new plant type • QTLs, quantitative trait loci • RILs, recombinant inbred lines • SLA, specific leaf area • SLN, specific leaf N • TDW, aboveground dry weight


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
THE STABLE carbon isotope ratio ({delta}13C) in plants, which is largely based on carbon isotope discrimination (CID) against 13C/12C by leaves during photosynthesis, has been used as a valuable index for cumulative Ci/Ca signature in a leaf, higher transpiration efficiency, and productivity under water limited conditions (Farquhar and Richards, 1984; Rebetzke et al., 2002). It has been suggested that higher CID was associated with higher yield under well-watered conditions in crops such as wheat (Triticum aestivum L.) (Condon et al., 1987), durum wheat (Triticum turgidum L.) (Araus et al., 2003), and peanut (Arachis hypogaea L.) (Wright et al., 1993). Under nonlimiting water conditions with flooded soils, biological and grain yield of rice were both positively correlated with CID (Kondo et al., 2004). These findings suggest that it is important to examine the mechanisms responsible for the physiological and genetic associations between CID, yield, and biomass productivity under both water limited and well-watered conditions in crops including rice.

Genotypic variation in CID was reported among rice groups; the japonica types showed lower CID or high {delta} 13C values compared with the indica types (Samejima, 1985; Dingkuhn et al., 1991; Peng et al., 1998; Kondo et al., 2004) suggesting that CID is strongly affected by genetic factors. Genotypic variation in CID was found in a number of studies that dealt with the CID and its correlation with other physiological traits (Condon et al., 1990; Johnson, 1993; Geber and Dawson, 1997; Saranga et al., 1999). Despite the number of studies dealing with genotypic variation in CID and its association with other physiological and yield-related traits, the physiological basis and genetic information to explain such associations are still lacking. Genotypic variation in CID is possibly caused by two factors, that is, leaf conductance to CO2 and CO2 incorporation (Farquhar et al., 1982). Identifying morphological and physiological factors, particularly leaf characters, related to the processes that determine genotypic variation in CID is essential in evaluating the value of CID as a criterion either for transpiration efficiency, productivity, or both.

Using molecular marker techniques, information on genetic bases for a large number of quantitatively inherited traits related to yield and other agronomic and physiological traits of crops has accumulated. In rice, a number of reports focused on genetic factors related to yield and yield components (Lin et al., 1996; Xiao et al., 1996; Lu et al., 1997; Zhuang et al., 1997; Yan et al., 1998; Ishimaru et al., 2001b; Ishimaru, 2003; Cui et al., 2003), panicle number (Liao et al., 2001), plant height (Li et al., 1995; Yan et al., 1998; Yu et al., 2002; Ishimaru et al., 2004), and growth duration (Yano et al., 1997). Except for a limited number of reports on leaf N (Ishimaru et al., 2001a) and photosynthetic rate (Teng et al., 2004), little information is available on the genetic factors that govern physiological functions of leaf traits related to photosynthesis. Quantitative trait loci for {delta}13C in crops such as soybean [Glycine max (L.) Merr.], cotton (Gossypium hirsutum L.), and barley (Hordeum vulgare L.) have been reported (Handley et al., 1994; Specht et al., 2001; Teulat et al., 2002; Saranga et al., 2004). In rice, while CID is highly affected by genotypic factor, very little effort has been directed toward understanding its genetic basis and its association with related plant traits and biomass production. Although QTLs for {delta}13C have been reported (Price et al., 2002; Ishimaru et al., 2001b), their association with other traits related to photosynthesis and productivity under lowland irrigated condition is not known. In addition, the effects of growth stage, plant part, and growing conditions on QTL for {delta}13C have not been examined.

In this study, we analyzed QTLs of 101 recombinant inbred lines (RILs) derived from a cross of IR69093–41–3–2 (japonica) and IR72 (indica) to identify QTLs controlling {delta}13C and examine their genetic relationship with other related traits at different growth stages for 4 yr.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Plant Materials and Field Experiments
The population consisted of 101 RILs derived from a cross between a lowland tropical japonica, IR69093–41–3–2 (herein referred to as new plant type [NPT]), and a lowland indica variety, IR72 (E.A. Barlaan, H. Sato, H. Hirabayashi, R. Ikeda and T. Imbe, unpublished data). The NPT was derived from a cross between IR65600–1–2–3 and Gundil Kuning, a tropical japonica. This population was chosen because the NPT and IR72 were found to have contrasting {delta}13C values from a previous study (Kondo et al., 2004). The RILs, IR72, and NPT were tested for 4 yr in 2001 (F5), 2002 (F6), 2003 (F7), and 2004 (F7) at the lowland experimental field (Fluvaquents, pH 5.2) of the National Institute of Crop Science, Yawara, Ibaraki, Japan under continuous irrigated lowland condition. About 25-d-old seedlings of each line were transplanted at one plant per hill at a spacing of 15 cm between plants and 30 cm between rows with two replications. Plot size was 2.3 m2 (three plant rows of 2.55 m). Transplanting was done on 10 May 2001, 15 May 2002, 21 May 2003, and 6 May 2004. Nitrogen was applied as basal at 80 to 100 kg ha–1 in the form of controlled-release urea. Phosphorus as single superphosphate and K as KCl at 50 kg ha–1 each were applied as basal fertilizer. The soil was kept under submerged conditions during the entire growth period.

Plant Sampling and Measurements
For each RIL and parents, grain samples were taken at maturity from 2001 to 2004. In 2003 and 2004, shoots were also sampled at maturity. Leaf and stem samples were taken at midgrowth stage on 7 Aug. 2003 and on 28 June 2004. In 2004, specific leaf area (SLA) was determined on the topmost fully expanded leaf based on leaf area, measured by a leaf area meter (Hayashi Denko Co., Tokyo, Japan), and on leaf dry weight at midgrowth stage. Specific leaf N (SLN) was calculated based on SLA and N content. Leaf SPAD value was measured using SPAD-502 chlorophyll meter (Soil–Plant Analysis Development [SPAD] Section, Minolta Camera Co., Osaka, Japan) on the topmost fully expanded leaf on 23 July 2004 with at least three leaves per plot. At maturity, plants were harvested to determine yield components and dry weight. All plant samples were oven-dried at 70°C to determine dry weight, {delta}13C, and N content. Grain yield was expressed as dry weight of filled grains. Dry weight of aboveground parts (TDW) was calculated as the summation of dry weights of all the parts of shoot and grain. Oven-dried samples for {delta}13C analysis were finely ground to a powder using a ball mill.

Carbon Isotope Analysis
The stable isotopic composition of plant samples was analyzed by an isotope ratio mass spectrometer connected to an elemental analyzer (Delta Plus XP, ThermoFinnigan Co., Bremen, Germany). Standardization and calibration followed the procedure of Zhao et al. (2004).

Linkage Analysis and QTL Mapping
Genetic correlation among {delta}13C values across year, stages, and plant parts and other related traits was determined as follows (Kearsey and Pooni, 1996):

Formula
where rG is genetic correlation between trait A and B, {sigma}Gab is genetic covariance between trait A and B, and {sigma}2Ga and {sigma}2Gb are genetic variance of trait A and B, respectively.

A molecular map with 182 markers (167 RFLP and 15 SSR markers) previously constructed (E.A. Barlaan, H. Sato, H. Hirabayashi, R. Ikeda, and T. Imbe, unpublished data) was used to analyze the QTL. A rice linkage map was constructed using Mapmaker/EXP version 3.0b (Lander et al., 1987). Composite interval mapping was conducted using the software Windows QTL Cartographer version 2.0 (Department of Statistics, North Carolina State University, Raleigh, NC) to analyze QTL for {delta}13C values and other related traits. A logarithm of the odds (LOD) score greater than 2.4, approximately corresponding to a probability at P = 0.05 with 1000 times permutation, was employed to declare the presence of putative QTL. Likewise, the additive effect and percentage of phenotypic variance associated with a QTL were calculated.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Climatic Conditions and Growth Duration
Climatic conditions and days to heading (DTH) of RILs in 4 yr are shown in Table 1. The mean temperature and solar radiation were highest in 2004 and lowest in 2003. Averaged across 4 yr, the NPT had 6 longer days to heading than IR72 (Table 1). In each year, the mean heading period of the RILs was longer by 6 to 10 d relative to the mean of the parents. The RILs had longest DTH in 2001 and 2003 ranging from 139 to 147 d.


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  		Table 1. Climatic conditions during growing period and days to heading from 2001 to 2004.

 
Phenotypic Variation
Across years, {delta}13C values of the NPT were consistently higher (indicating lower CID) by 1.6 to 2.8{per thousand} than those of IR72 (Table 2). Grain {delta}13C value of RILs was –28.2{per thousand} on the average across 4 yr and varied by 0.4{per thousand}. In the parents and RILs, grain {delta}13C values were generally higher than the shoot value at maturity. The leaf showed lower values than the stem at midgrowth stages. Across years, stage, and parts, {delta}13C values among RILs showed significant genetic correlation with each other (Table 3), indicating that {delta}13C values were largely affected by genetic factors. In particular, correlation was strong among plant parts at midgrowth stage and tended to be weaker between stages.


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  		Table 2. Values of {delta} 13C ({per thousand}) of IR72, new plant type (NPT), and recombinant inbred lines (RILs) across parts and years.

 

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  		Table 3. Genetic correlation among {delta}13C in different years and parts.

 
The SPAD value was higher in the NPT than in IR72 (Table 4), which was associated with higher leaf N content and lower SLA in the NPT than in IR72. The mean SPAD values of the RILs were closer to that of IR72 whereas the maximum values were comparable with that of the NPT. Leaf N content varied largely among RILs by 2.5% in 2003 and by 1.9% in 2004. Large variations in SLA among RILs were also observed.


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  		Table 4. Agronomic and physiological traits of IR72, new plant type (NPT), and recombinant inbred lines (RILs) in 2003 and 2004.

 
The parents showed contrasting plant stature with higher panicle number and lower plant height for IR72. Dry weight of aboveground parts and harvest index (HI) did not differ largely between the parents in 2004. Panicle number, plant height, TDW, and HI varied largely among the RILs.

The frequency distributions of {delta}13C values in the top leaves in 2004 showed normal distribution with values of skewness and kurtosis < 1.0 (Fig. 1 ). Most RILs showed {delta}13C values between parents and only 1% of RILs outperformed the parents.


Figure 1
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  		Fig. 1. Phenotypic distribution of {delta}13C of top leaves at midgrowth stage of recombinant inbred lines grown under irrigated lowland conditions in 2004. Arrows indicate values of the parents, IR69093–41–3–2 (new plant type) and IR72.

 
Interrelationship between {delta}13C and Related Traits
Genetic correlation of the {delta}13C value with other traits is shown in Table 5 for 2001 to 2003 and Table 6 for 2004. Values of {delta}13C at maturity, but not those at midgrowth, were negatively correlated with yield and HI in 2003 and 2004. The grain {delta}13C values and grain N content showed positive correlation in all years except in 2002. The {delta}13C value of the top leaf was negatively correlated with SLA and leaf N content at midgrowth stage in 2004.


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  		Table 5. Genetic correlation of {delta}13C with other agronomic and physiological traits from 2001 to 2003.

 

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  		Table 6. Genetic correlation of {delta}13C with other agronomic and physiological traits in 2004.

 
Genetic correlation of yield with other traits is shown in Table 7. The negative correlation of yield with DTH was associated with the negative correlation between HI and DTH. Total dry weight of aboveground parts showed positive correlation with DTH in 2004 indicating that a longer growth period was associated with higher biomass production. Yield was negatively correlated with N content of shoot and grain at maturity.


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  		Table 7. Genetic correlations of yield, aboveground dry weight (TDW), and harvest index (HI).

 
Mapping of QTLs for {delta}13C and other Related Traits
Putative QTLs detected for {delta}13C are listed in Table 8. The location of QTL for {delta}13C and other traits are shown in Fig. 2 . Across years, stages, and plant parts, QTLs for {delta}13C were detected on chromosomes 2, 4, 8, 9, 11, and 12. No QTL was detected for the shoot at maturity in 2003. Except for QTLs on chromosomes 2 and 9, the alleles from the NPT increased the {delta}13C value. The contribution of individual QTLs to the total variation varied from 7.6–19.0%. The QTLs near marker G148 to G2140 on chromosome 12 were detected across plant parts at midgrowth stages in 2003 and 2004. The QTLs for {delta}13C in top leaves on chromosome 12 contributed 17.6% to the total variation in 2004. The QTLs for {delta}13C in the shoot at maturity were also detected on chromosome 12 near marker G2140 in 2004. In 3 out of 4 yr, QTLs for {delta}13C of grains were commonly found near RM444 on chromosome 9.


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  		Table 8. QTLs for {delta}13C in different years, plant parts, and stages.

 

Figure 2
Figure 2
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  		Fig. 2. Likelihood intervals for QTLs associated with {delta}13C and other traits detected from 2001 to 2004. Abbreviations: {delta}13CG, {delta}13C in grain; {delta}13CS, {delta}13C in shoot; DTH, days to heading; FG/Pan, filled grain number/panicle; GY, grain yield; HI, harvest index; %NG, grain N content; %NL, N content in leaf; %NS, N content in shoot; %NSt, N content in stem; %NStLL, N content in stem + lower leaf; %NTL, N content in top leaf; NUp, N uptake; PH, plant height; PN, panicle number; SLA, specific leaf area; SLN, specific leaf N; TDW, aboveground dry weight; TGW, 1000-grain weight 01 to 04 indicate year. M and MG indicate traits measured at maturity and midgrowth stages, respectively. + and – indicate the positive and negative effect of QTL on the value with alleles from IR69093–41–3–2 (new plant type), respectively.

 
Details of QTLs for traits other than {delta}13C are listed in Table 9. In 2004, QTLs for SPAD were detected on chromosomes 4 (C891), 7 (C847), and 11 (C950). The QTL on chromosome 4 (C891) had a strong effect explaining 22.1% of the total variation and overlapped in a similar region with that of a QTL for {delta}13C in the stem. The QTLs for SPAD on chromosome 4 (C891) and 7 (C847) were overlapped with the QTLs for SLN. Two QTLs for SLA were detected on chromosomes 5 (C1018) and 8 (C502) which increased SLA by the NPT alleles. The QTLs for SLN and SLA were overlapped on chromosome 8.


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  		Table 9. QTLs for agronomic and physiological traits in 2001 to 2004.

 
Leaf N content in top leaves at midgrowth stage in 2004 had four QTLs on chromosomes 1 (RM212), 5 (R1553), 9 (C709B), and 11 (C477) contributing from 9.0 to 16.9% to total variation, and all of which increased N content by the NPT allele. Leaf N content at midgrowth stage in 2003 had two QTLs on chromosomes 2 (C560) and 4 (C107), which increased leaf N by the alleles from IR72. The QTLs for shoot N content at maturity were detected on chromosomes 2 (C560), 3 (R1927), and 8 (R1813) in 2003 and on chromosomes 7 (R2829), 9 (C1227), and 10 (R716) in 2004. The QTL for grain N content was detected repeatedly on chromosome 8 (G1073) from 2002 to 2004, and the NPT alleles increased N content. This QTL explained 10.0 to 15.9% of the total variation in grain N content. The QTL for N uptake at maturity was detected on chromosome 10 (C809) in 2003, which explained 9.6% of the total variation. In 2004, two QTLs for N uptake were detected on chromosome 3 (R1925 and R2170).

QTL for Productivity
For TDW at maturity, two QTLs on chromosome 3 (R1925 and C563) and one QTL on chromosome 8 (C1121) were detected with maximum contribution of 23.5% to total variation in 2004. The QTLs on chromosomes 3 (C563) and 8 increased TDW by the NPT allele, and the QTL near R1925 on chromosome 3 had the opposite effect. The QTL for TDW on chromosome 8 (C1121) was in a similar positions with that of the QTL for DTH in 2004. Likewise, the QTLs for TDW at maturity and DTH were also detected in similar positions on chromosome 8 in 2003. The QTL for TDW on chromosome 3 (R1925) overlapped with those for plant height and panicle number in 2004. The QTLs for plant height were detected on chromosomes 3, 4, and 8 at maturity.

In 2003, QTLs for yield were detected on chromosome 7 (C847) and 8 (G1073) and QTLs for HI were detected on chromosomes 1 (R596) and 8 (G1073). The QTLs on chromosome 8 for yield and HI were mapped on the same position and increased the values by the IR72 alleles. In 2004, QTLs for yield and HI were detected in a similar position on chromosome 11 (R3202 to R1466) which increased the value by the IR72 allele.

Four QTLs for panicle number were detected on chromosomes 3 (RM85), 4 (C1016), 9 (C1263), and 10 (R1877) and the alleles from IR72 increased panicles. The QTLs for 1000-grain weight were detected on chromosomes 2 (C601), 8 (G187), and 9 (C570) and those for the number of filled grains per panicle were detected on chromosomes 3 (R2847), 7 (R1789), and 10 (R1877). Some putative QTLs for 1000-grain weight and number of filled grain per panicle had an opposite effect.

Across 4 yr, QTLs for DTH were detected in a similar position on chromosome 8 (C1121), contributing an average of 21.5% to total phenotypic variation. This QTL prolonged DTH by the NPT alleles. Besides this QTL on chromosome 8, QTLs for DTH were also detected on chromosome 7 (R1789) in 2001, and on chromosomes 1 (C225) and 12 (G148) in 2004.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Variations in {delta}13C and other Traits across Years
Values of {delta}13C were consistently higher in the NPT than in IR72 across years, plant parts, and stages. Our result was consistent with previous findings, which showed that the indica genotypes generally have lower {delta}13C (Samejima, 1985; Dingkuhn et al., 1991; Kondo et al., 2004). The parents in the present study showed quite contrasting {delta}13C values when we compared the differences in their {delta}13C values with those of previous genotypic comparison results using 11 genotypes (Kondo et al., 2004). The value of {delta}13C was lower in the assimilating organs and highest in grain, which was consistent with the previous reports in rice (Kondo et al., 2004) and other crops (Farquhar and Richards, 1984; Acevedo, 1993; Saranga et al., 1999).

The difference in {delta}13C among RILs was relatively consistent among plant parts, stages, and years. At midgrowth stages, close genetic correlations existed among plant parts. In general, weaker genetic correlations were observed between midgrowth stage and maturity than among plant parts within the same stage. This finding indicates that the change in {delta}13C along with growth stages differs among RILs.

General Trend in QTL for {delta}13C
Results of QTL analysis showed that {delta}13C was controlled by several QTLs with relatively small effects contributing to less than 20% of total variation, indicating that the genetic control of {delta}13C was relatively complex as reported in other crops (Specht et al., 2001; Saranga et al., 2004). Significant regions affecting {delta}13C were identified on chromosomes 2, 4, 8, 9, 11, and 12 across plant parts, stages, and years. Out of these QTLs, those on chromosomes 2 and 9 decreased the {delta}13C value by the NPT allele, indicating that genes having both positive and negative effects were involved to determine the difference in {delta}13C between the NPT and IR72.

The location of QTLs for {delta}13C was affected by plant part, growth stages, or both. Most of the QTLs for {delta}13C detected for the assimilating organs were found on chromosomes 4 and 12, whereas the QTLs for grain at maturity were repeatedly detected on chromosome 9. These findings suggest that the expression of QTLs for {delta}13C values differs during crop development. The difference in {delta}13C between the assimilating organs before heading and grain at maturity was possibly attributed to the difference in growth stage and chemical components. The {delta}13C values in grain at maturity probably reflects, to some extent, the {delta}13C value in the carbon assimilated during the later growth stage, because carbon in the grain is derived from the newly assimilated carbon after heading and from the stored carbon in stem and sheath at heading, the former being usually the major component. In addition, the significance of 13C/12C fractionation in the course of synthesis for starch (Scott et al., 1999) and other major components in the grain should be clarified further to explain the different {delta}13C between grain and shoot and their genetic variation. In addition, there were QTLs for {delta}13C which were not detected consistently among years. The effect of growing conditions on QTLs for {delta}13C needs to be clarified (Price et al., 2002; Teulat et al., 2002).

In 2002, the regions of QTL for grain {delta}13C found on chromosome 11 (C1172) were similar to those detected by Ishimaru et al. (2001b) who used the BC1 population of Nipponbare (japonica) and Kasalath (indica). Both QTLs increased the value by the japonica alleles. Other QTLs detected for {delta}13C in grain in this study were not consistent with Ishimaru et al. (2001b). These comparisons indicate that common and unique QTLs are responsible for the differences in {delta}13C between the indica and japonica varieties among the populations.

Association of QTL for {delta}13C and Other Leaf-Related Traits
Some QTLs for {delta}13C and other traits were located in the same region or a similar position. The occurrence of QTLs associated with different traits in the same locus may be explained by the fact that (i) the QTLs are closely linked genetically or (ii) a single locus controls multiple traits and a gene may have pleiotropic effects.

One of our final interests is to clarify the mechanisms by which each QTL genetically controls the {delta}13C value. Higher {delta}13C (lower CID) can be a result of lower Ci/Ca brought about by lower leaf CO2 conductance, greater CO2 incorporation capacity, or both (Farquhar et al., 1982). Among the QTLs for {delta}13C, none was clearly co-located with the QTLs for other traits, except the QTL near marker C558 on chromosome 4. The QTLs on chromosome 4 for {delta}13C values in stem at the midgrowth stages in 2003 were overlapped with QTLs for SPAD and SLN in 2004. These QTLs for {delta}13C, SLN, and SPAD had the effect of increasing the values for the NPT alleles. The QTL for {delta}13C in the leaf was also detected on the same position although the effect was weak (LOD = 2.08). These indicated the possibility of genetic association of {delta}13C values with N content, leaf thickness, or both. However, further study is obviously needed to examine this possibility.

The QTLs for {delta}13C in leaf and stem at midgrowth stages were repeatedly detected in a similar position on chromosome 12 in 2003 and 2004. These QTLs were probably related to the {delta}13C from the carbon assimilated at the early growth stages. However, the function of the these QTLs could not be elucidated in this study because no QTL for other traits was co-located in a similar region.

It has been reported that the genotypic variation in {delta}13C value in rice was related to stomatal conductance (Dingkuhn et al., 1991; Kondo et al., 2004). Although genotypic variation in stomatal conductance and morphology has been recognized in rice (Maruyama and Tajima, 1990), only a limited number of studies were conducted on the genetic control. The QTLs for stomatal frequency (Ishimaru et al., 2001c) and stomatal resistance (Teng et al., 2004) were not overlapped with any QTLs for {delta}13C found in our study.

Nitrogen-Related Traits
It is known that leaf N and Rubisco contents strongly affect photosynthesis (Mae, 1997; Makino, 2003). About 50% of total soluble protein and 25% of total N are in Rubisco protein in rice leaves (Makino, 2003). The QTLs for N content in the leaf at midgrowth and in the shoot at maturity were co-located on chromosome 2 with positive effect of increasing the values for the IR72 alleles in 2003 and on chromosome 9 with positive effect of increasing the values for NPT alleles in 2004. In a similar region on chromosome 9, Ishimaru et al. (2001a) reported QTLs controlling protein and Rubisco content in the rice leaf. The locations of QTLs for N content in shoot at midgrowth and maturity were not consistent between 2003 and 2004. The QTL for grain N content on chromosome 8 (G1073) was detected consistently across 3 yr, explaining 15.9% of total variation at the maximum. These findings suggest that grain N accumulation is affected by genetic factors more than shoot N. The QTLs for N uptake and TDW were overlapped on chromosome 3 (R1925) in 2004 indicating the possibility that these physiologically related traits were genetically linked or under control of genes having pleiotropic effects.

Biomass Production and Yield
Growth duration and plant stature such as plant height and panicle number are important prerequisites to attain the desired TDW and yield level (Yoshida, 1981). In this study, the QTLs for TDW at maturity and DTH were detected in a similar position on chromosome 8. Both QTLs had the effect of increasing the value by the NPT allele. One major QTL for heading date, Hd5, was previously mapped on chromosome 8 in a similar position (Yano et al., 1997).

At maturity, the QTL for plant height was found near the position of the QTLs for TDW and DTH on chromosome 8 in 2004. Other studies also showed QTLs for plant height in a similar region on chromosome 8 (Li et al., 1995; Xiao et al., 1996; Lu et al., 1997; Ishimaru et al., 2004). On chromosome 3, QTLs for plant height and panicle number were co-located with QTL for TDW near marker R1925. It is needed to further clarify whether or not TDW was genetically linked to plant height and panicle number.

Grain yield of rice is a function of biomass accumulation and the amount of carbohydrates translocated to the grain during the grain-filling period (Yoshida, 1981). The fact that HI and yield tended to decrease with longer DTH indicated that RILs with longer duration may have lower HI partly due to lower grain filling caused by low temperature after September since both the parent varieties were of tropical origin. QTLs for yield and HI were co-located in similar regions on chromosome 8 (G1073) in 2003 and on chromosome 11 (R3202 to R1466) in 2004. These common QTLs for yield and HI had the effect of increasing the values by the IR72 alleles. It is generally known that indica varieties have higher grain-filling ability than japonica varieties (Miah et al., 1996; Peng et al., 1999). It would be interesting to verify how the QTLs for yield and HI are related to this difference in grain-filling abilities between the indica and japonica varieties.

{delta}13C and Productivity
The results on genetic correlation indicated an association of lower {delta}13C value with higher yield and HI, and lower N content at maturity. The association between higher yield and lower grain N content was reported for wheat (Groos et al., 2003). Phenotypic negative relationships of {delta}13C with HI and yield have been observed in rice and other crops under favorable water supply (Acevedo, 1993; Fischer et al., 1998; Wright et al., 1988; Araus et al., 2003; Kondo et al., 2004). A possibility for genetic association between {delta}13C and HI was indicated in cowpea [Vigna unguiculata (L.) Walp.] (Menendez and Hall, 1996). In this study, the mechanism underlying genetic association of {delta}13C with HI and yield could not be clarified. The lower {delta}13C value and higher yield may be linked through larger leaf stomatal conductance supported by favorable leaf water status, stronger sink strength, or both (Fischer et al., 1998). The {delta}13C value at maturity had closer correlation with HI and yield than the {delta}13C value at midgrowth stages. Further analysis on separating the {delta}13C signature at ripening stage from those before heading would provide a clearer insight.

Genetic associations of {delta}13C or transpiration efficiency with productivity were studied in crops grown under water-limited conditions (Saranga et al., 2004; Specht et al., 2001). Rice grown under flooded conditions would offer an interesting contrast in the study of genetic and physiological linkage of {delta}13C with productivity. This study reveals the overall feature of the genetic basis for {delta}13C. Further study is underway to elucidate the actual functions of QTLs for {delta}13C expressed among different growth stages to understand fully the effects of such QTLs on productivity.


   ACKNOWLEDGMENTS
 
This work was partly supported by the Japan Society for Promotion of Science (JSPS). We thank Dr. Y. Uga (National Institute of Agrobiological Sciences), Drs. Y. Takeuchi and H. Hirabayashi (National Institute of Crop Science) and Dr. K. Ise (Japan International Research Center for Agricultural Science) for their valuable advice on QTL analysis and statistical analysis. We also thank Ms. N. Teranuma of the Ibaraki Agricultural Center for her technical assistance.

Received for publication June 6, 2005.


   REFERENCES
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 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
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