Euphytica 140: 155–162, 2004. C 2004 Kluwer Academic Publishers. Printed in the Netherlands.
155
QTL analysis of seed dormancy in rice (Oryza sativa L.) Longbiao Guo1,2 , Lihuang Zhu3 , Yunbi Xu4 , Dali Zeng2 , Ping Wu1,∗ & Qian Qian2,∗ 1
College of Life Science, Zhejiang University, Hangzhou 310029, P.R. China; 2 State Key Lab for Rice Biology, China National Rice Research Institute, Hangzhou 310006, P.R. China; 3 Institute of Genetics, China Academy of Sciences, Beijing 100101, P.R. China; 4 Department of Plant Breeding, Cornell University, Ithaca, New York 14853-1901, U.S.A.; (∗ author for correspondence: e-mail:
[email protected])
Received 20 July 2004; accepted 18 August 2004
Key words: double haploid (DH) population, quantitative trait loci (QTL), rice (Oryza sativa L.), seed dormancy Summary Effective cumulative temperature (ECT) after heading would be a more reasonable parameter for seed sampling of pre-harvest sprouting/seed dormancy (SD) tests in segregating populations than the days after flowering. SD is an important agronomic trait associated with grain yielding, eating quality and seed quality. To identify genomic regions affecting SD at different grain-filling temperatures, and to further examine the association between SD and ECT during grain-filling, 127 double haploid (DH) lines derived from a cross between ZYQ8 (indica)/JX17 (japonica) by anther culture were analyzed. The quantitative trait loci (QTLs) and their digenic epistasis for SD were identified using a molecular linkage map of this population. A total of four putative QTLs for SD (qSD-3, qSD-5, 6 and 11) were detected on chromosomes 3, 5, 6 and 11, together explaining 41.4% of the phenotypic variation. Nine pairs of digenic epistatic loci were associated with SD on all but chromosome 9, and their contributions to phenotypic variation varied from 2.87%–8.73%. The SD QTL on chromosome 3 was identical to the QTLs found in other mapping populations with different genetic backgrounds, which could be a desirable candidate for gene cloning and marker-assisted selection in rice breeding.
Introduction Seed dormancy (SD) is an important agronomic trait associated with grain eating quality and seed quality (Hu et al., 2003). There are significant correlations between SD and pre-harvest sprouting (PHS), and genotypic difference in SD (Anderson et al., 1993; Chang & Yen, 1969; Osa et al., 2003; Li et al., 2004). In crop production SD has advantages as well as disadvantages. For succeeding crops and accelerating breeding processes, the crop cultivars or breeding materials need to be sown for a second/next crop quickly (Seshu & Sorrells, 1986). For grain quality, however, the cultivars with moderate dormancy are needed to protect the grains from germinating before harvesting. In southern China, due to the long spell of rainy weather in early summer and autumn, it causes heavy PHS in the field for more than 6% of the rice acreage, which could be up to 20% for hybrid rice (Hu et al., 2003). Therefore,
understanding of the genetic bases for SD is a major concern for both geneticists and plant breeders to solve the problem with PHS. SD is the failure of the fully mature and viable seed to germinate to an appreciable degree under favorable environmental conditions. The expression of dormancy in crop is influenced by both environment and genetic factors, such as rudimentary or physiologically immature embryos, mechanically resistant or impermeable seed coats, and the presence of endogenous germination inhibitors (Li & Foley, 1997). Mechanisms may involve the expression of certain genes, levels of certain plant growth regulators, the activity of important respiratory pathways or the mobilization and utilization of food reserves (Adkins et al., 2002). PHS in rice represents a major constraint to the production of highquality grain. Genetic variation for tolerance to PHS is associated with SD. SD is a complex trait controlled by polygenes with effects modified by the genetic
156 background and environmental factors (Anderson et al., 1993). A major approach to determine the genetic architecture for SD is to dissect it into quantitative trait loci (QTLs). Recently many QTLs affecting SD and PHS tolerance have been identified in various plant species such as barley (Oberthur et al., 1995; Larson et al., 1996; Han et al., 1996; Li et al., 2004; Thomas et al., 1996), wheat (Anderson et al., 1993; Flintham et al., 2002; Kato et al., 2001; Roy et al., 1999; Zanetti et al., 2000), Arabidopsis (van der Schaar et al., 1997), and rice (Wan et al., 1997; Lin et al., 1998; Cai & Morishima, 2000; Dong et al., 2003; Miura et al., 2002). These studies have identified various genetic loci for SD and PHS, which in part reflect the different samplings from the available gene pools and indicate that many genes are involved in SD and PHS. However, it should be noted that QTLs in similar chromosomal locations were identified in various studies, which indicate similar alleles may control SD and PHS tolerance. SD and germination are processes that involve a great number of genes and are influenced by day length, humidity and temperature (Takahashi, 1997). Temperature during grain filling of rice affects the speed of seed maturation, which results in either seed dormancy or germination. The effective cumulative temperature (ECT), a difference between active temperature and developmental zero temperature of a crop, is a more stable parameter than the leaf-age interval or time-interval of parental lines used in the synchronization of flowering. ECT has been extensively applied in determining the ECT seeding interval of the parental lines from sowing to heading in hybrid rice production of China (Xie, 2002). Because ECT is a better parameter than the days for different varieties and temperatures, it would be more reasonable to harvest seed from a rice segregating population for germination test according to ECT after heading instead of the days after flowering (Xue et al., 2004). In addition, due to wide genetic diversity
of SD in rice germplasm resources, genetic mapping and comparison of the genomic regions associated with SD across commercial rice varieties need a further study. Our objective in the present study was to use molecular markers to identify genomic regions affecting SD, and to further examine the association between SD and ECT using a DH population derived from anther culture of a typical indica/japonica hybrid, ZYQ8/ JX17.
Materials and methods Plant materials A double haploid (DH) population consisting of 127 lines derived from a cross between a typical indica variety Zhaiyeqing 8 (ZYQ8) and a typical japonica Jingxi 17 (JX17) (Zhu et al., 1993) was used in the study. Mean temperature and ECT from the flowering to maturity during the germination tests in 2002 were showed in Tables 1 and 2. Three panicles from each DH line were harvested when their ECT reached 600 ◦ C after flowering (Xue n et al., 2004). ECT was calculated by using K e = i=1 (Ti − T0 ), where Ke is ECT, Ti the mean temperature on the ith day and T0 developmental zero temperature.
SD phenotyping The 127 lines and their parents, ZYQ8 and JX17, were evaluated at the experimental station of China National Rice Research Institute, Hangzhou, China. The field planting followed a randomized complete block design with two replications. The germinated seeds were sown in a seedling bed on May 23, 2002, and the seedlings were transplanted to a paddy field 27 days later. Two parents and 127 DH lines were planted in 3 rows with
Table 1. Mean temperature and effective cumulative temperature (ECT) during ten-day intervals from flowering to maturity in 2002
Stage MT (◦ C)/d ECT (◦ C)/10d
Late July
Early August
Middle August
Late August
Early September
Middle September
Late September
31.6
27.3
25.0
28.9
27.5
24.5
21.4
216.4
172.4
150.2
189.2
175.4
145.3
113.9
MT – mean temperature.
157 Table 2. ECT and the days in DH lines required from flowering to maturity in 2002 The days after flowering (d)
ECT during grain-filling ( ◦ C)
DH lines
Species
Heading date
DH32
Indica
14, July
28
600
DH67
Indica
6, August
36
600
DH94
Japonica
4, September
Mean
43
600
36
600
8 hills per row, spacing at 16 cm × 23.1 cm. The six plants from the middle of the three row in each replication were sampled to score for germination rate, and three panicles were collected from each plant when ECT reached 600 ◦ C after heading and were immediately placed under conditions of 30 ◦ C and 100% relative humidity for 7 days. Germination test was done with the instrument Enviros KCH-1000 (EYELA Instrument Factory, Japan). Germination was evaluated visually by protrusion of the radicle from the hull by 2 mm. SD was evaluated in terms of germination rate and scored as a percentage of germinated seeds. To normalize the variances, the percentage germination rate of each DH line was 1 transformed to the arc sine [= arc sine (χ ) 2 ] and the transformed data were used for QTL analysis.
Results
QTL analysis
Relationship between seed dormancy and effective cumulative temperature
Linkage map containing a total of 160 restriction fragment length polymorphism (RFLP) and 83 simple XXX (SSR) markers distributed on all 12 rice chromosomes were selected to construct a rice linkage map using Mapmaker/EXP version 3.0 as described previously (Lu et al., 1996; Xu et al., 1998). Of SSR markers, these mapped only in the present population were denoted as GAXX, CTXX, ATTXX and TCTXX (Xu et al., 1998), whereas others were named as RMXX by Chen et al. (1997). QTLs and their digenic interaction for SD were detected by interval mapping using the software Mapmaker/QTL version 1.1 (Lander & Botstein, 1989; Lincoln et al., 1993) and QTLMapper 1.0 (Wang et al., 1999). The presence of a QTL was claimed when a LOD score is larger than 2.4. And for declaring digenic epistatic loci, a LOD of 2.7 (corresponding to a probability of 0.001) was selected as the threshold. Genetic parameters such as explained variation and genetic effect of each QTL were estimated. QTLs were named following the nomenclature of McCouch et al. (1997).
Variation in seed dormancy between parents and among the DH population SD in the two parents (ZYQ8 and JX17) was showed in Figure 1. JX17 had significantly higher SD (76.93%) than ZYQ8 (12.84%) (P < 0.01). In the DH population, SD showed a two-peak distribution with big transgressive segregation over the two parents (Figure 1), indicating the quantitative inheritance. Due to the distribution significantly departed from normality, the SD data were transformed by the arc sine [= arc sine (χ ) 12 ] for the subsequent QTL analysis.
The days for harvesting after flowering in the DH population, when the ECT reached 600 ◦ C, ranged from 28 days to 43 days. ECT and the days from flowering to maturity in some DH lines were shown in Table 2. The correlation between SD and the harvest date was not significant (r = 0.26).
Figure 1. Distribution of seed dormancy in the DH population.
158 Table 3. Putative QTL of seed dormancy in rice Locus
Chromosome
Marker interval
LOD score
Variance explained (%)
Additive effect (%)
5.11
14.5
−10.9∗
qSD-3
3
CT339-G62
qSD-5
5
RG776B-RM164
2.50
7.3
8.9
qSD-6
6
G329-RG244
2.50
7.5
9.2
qSD-11
11
RZ638-G320
3.17
12.1
10.4
*Additive effect of ZYQ8 allele by arc sine of germination rate.
QTLs for seed dormancy The results of QTL analysis were shown in Table 3. Four putative QTLs (qSD-3, qSD-5, qSD-6 and qSD11) for SD were detected on chromosomes 3, 5, 6 and 11, respectively (Figure 2). The additive effects of alleles from the parents in the four QTLs ranged from 8.9%–10.9% in the arc-sine transformation of germination rate. JX17 alleles in three putative QTLs from
chromosomes 5, 6, and 11 and ZYQ 8 allele from chromosome 3 increased the germination rate. Total phenotypic variation explained by these four putative QTLs was 41.4%. Digenic epistasis for seed dormancy Nine pairs of digenic interaction for SD were identified on all except for chromosome 9 (Table 4). Their
Figure 2. QTL map for seed dormancy in DH population. Four QTL for SD detected in this study, and the QTL identified on chromosome 3 by Lin et al. (1998 ), Cai & Morishima (2000) and Wan et al. (1997 ) were integrated into this map. The markers significantly associated with SD, C62, RZ329 and Pgi 1, located at about 52.3 cM, 53.3 cM and 90.8 cM, respectively.
159 Table 4. Digenic interactions identified for rice seed dormancy in ZYQ8/JX17 DH population LOD
AAija (%)
Varianceb (%)
CT442-RG167
2.97
−0.21
7.65
CT339-G62
4.61
0.12
3.76
5
RG776B-RM164
3.82
−0.19
2.87
7
CT360-G379A
6.28
−0.25
8.73
G318-CT563
4.52
−0.25
5.72
GA53-C746
2.71
−0.18
4.01
GA376-CT195
4.67
0.18
4.13
12
RG463-RG323
5.02
−0.23
6.21
10
G2155-C16
4.55
0.19
5.17
Chromosome
Interval i
Chromosome
Interval j
1
G370-C385
11
1
G370-C385
3
1
G370-C385
2
GA43-G243A
2
RG322-CT41
4
3
C63-CT125
3
3
CT339-G62
8
3
G249-G164
6
G329-RG244
a “Additive × additive” effect: the positive value indicates that the two-locus genotypes being the same as those in parent ZYQ8 (or JX17) take the positive effects, while the two-locus recombinants take the negative effects. The case of negative value is just the opposite. b Variance explained by each pair of epistatic loci.
epistatic effects ranged from 0.12%–0.25% in the arc-sine transformation of germination rate, explaining 2.87%–8.73% of total variation. Only one pair of epistasis happened between two marker intervals locating on the same chromosome, and the rest of interaction locating on different chromosomes. Four pair of epistasis happened between a marker interval with significant main-effect and a marker interval without significant main effect. No epistasis happened between two marker intervals both with significant main effects. CT339-G62 on chromosome 3 had significant interactions with two intervals on chromosomes 1 and 8. G370-C385 on chromosome 1 had significant interactions with three intervals on chromosomes 3, 5 and 11. Comparison of the mapped QTLs for seed dormancy with other reports The QTLs for SD in rice have been previously reported by Wan et al. (1997), Lin et al. (1998) and Cai & Morishima (2000) by using different populations under different genetic backgrounds and experimental conditions. The QTL on chromosome 3 was detected in all above three mapping populations reported and in this study, with genetic variation explained from 9%–25%. To facilitate the comparison of QTL locations, the QTLs detected in these experiments were aligned to the ZYQ8/JX17 map presented in this study (Figure 2). The regions of QTL identified by Cai & Morishima (2000), Lin et al. (1998) and Wan et al. (1997) were located at about 52.3 cM, 53.5cM and
90.8 cM, respectively, although all of them need to be fine mapped.
Discussion Pre-harvest sprouting (PHS) happened heavily in moist conditions or the long spell of rainy seasons. Ikehashi (1972) and Wan et al. (1997) reported that the temperature during the grain-filling affects PHS and SD. High temperature could accelerate seed maturity. The days from flowering to harvesting seed also directly affect the expression of PHS and SD (Gu et al., 2004). Therefore, it is important to determine when the seed sample should be collected or harvested from the plants in segregating populations. Previously, Lin et al. (1998) and Gu et al. (2004) harvested the seed after 35 days and 40 days of flowering. But in a segregating population with significant difference in heading dates can be detected. In the present DH population, DH32, an indica line, when headed in high temperature, took a shorter time, 28 days, to mature, while, DH94, a japonica line, when headed in low temperature, took a longer time, 43 days, to mature. Grain-filling rates vary among indica/japonica lines or under different temperatures, but the ECTs after flowering in DH lines are near 600 ◦ C (Xue et al., 2004). So we used ECT after flowering to determine when the seed is sampled for germination test. It would be more reasonable that harvesting seeds for SD test based on ECT after flowering than other methods as suggested by Yasue & Asai (1968), Lin et al. (1998) and Gu et al. (2004).
160 In this study, SD showed a two-peak distribution with transgressive segregation over the parents. The distribution that significantly deviated from normality might be associated with fresh seed samples, and it needs to be confirmed, but fresh seeds used for germination test corresponded better to PHS in the field. Moreover, in this case the SD distribution was similar to the distribution of PHS in Asominori/IR24 RI lines under the natural growth condition (Dong et al., 2003), or to a combinant of two germination distributions at 1 and 11 days of after-ripening displayed by Gu et al. (2004) using the BC1 (EM93-1//EM93-1/SS18-2) lines. The results indicate that the germination distribution was associated with seed sampling time. SD is a complex trait in rice, and is controlled by multi-genes. Recent marker-based studies have identified many QTLs for SD or PHS by using seven populations (Gu et al., 2004). Wan et al. (1997) reported that five isozyme lociPgi1 (chr3), Amp3 andC (chr6), Est9 (chr7) andAcp2 (chr12) were associated with SD. Using RFLP markers, Lin et al. (1998) reported five loci on chromosomes 3, 5, 7 and 8 which were linked with SD. Using a RIL population derived from a common wild rice (O. rufipogen, W1944) and a cultivated rice (Indica, Pei-kuh), Cai & Morishima (2000) found QTLs for SD on all except for chromosomes 4 and 10. We identified four QTLs controlling SD in ZYQ8/JX17 population by using Mapmaker/QTL, which accounted for 41.4% of the total phenotypic variation in SD. These QTLs were also confirmed by the one-way ANOVA analysis (data not shown). The four SD QTLs identified in this study located closely to at least four found by Cai & Morishima (2000) and two by both Wan et al. (1997) and Lin et al. (1998). The unexplained variation might be due to environmental effects or to undetected QTLs with relatively smaller phenotypic effects. Although some corresponding QTLs were found from different rice populations, many others were populationspecific, indicating that there is great variation in SD in rice germplasm resources and elite resources were worth exploiting. Four DH lines with high SD from the current mapping population, DH53, DH70, DH80 and DH110, had been selected to backcross with their parents to construct near isogenic lines (NIL) in order to fine map and clone the SD QTL on chromosome 3. Epistases are involved in the regulation of genetic variation for SD. Additive-additive interaction includes three types: interaction between two marker intervals with significant main effects, interaction between a marker interval with significant effect and the other without significant effect, and interaction between two
marker intervals neither with significant effect (Guo et al., 2002). A chromosomal region marked by a marker without a significant effect on a quantitative trait may also contribute to the phenotypic variation by interaction with another marker locus (Li et al., 1997). In this study, nine pairs of digenic epistatic marker intervals for SD were identified on all except for chromosome 9. No epistatic locous was found between two marker intervals both with significant effects. Four pair of epistasis happened between a significant marker-interval and a non-significant marker-interval. The interval CT339G62 on chromosome 3 had simultaneously interactions with two intervals on chromosomes 1 and 8. The interval G370-C385 had simultaneously interactions with three intervals on chromosomes 3, 5 and 11. Interactions between two dormancy QTLs were previously detected in Arabidopsis, barley, wheat and rice (Anderson et al., 1993; Oberthur et al., 1995; Gu et al., 2004), which indicated the presence of a genetic complex network in the control of seed dormancy and the difficulty in breeding for favorable SD epistases. Beachell (1943), Tang & Chiang (1955) and Seshu & Sorrells (1986) reported great variation in rice seed dormancy. The japonica subspecies usually had shorter periods of dormancy than the tropical indica subspecies. Indica and japonica rice likely diverged from one another as long as 2 to 3 million years ago, which generally adapted to growth in different temperate regions and humidity conditions and increasingly formed many distinct characteristics between the subspecies in long evolutionary history, such as cold resistance, fertilizer tolerance, grain shape, and grain quality (Qian et al., 2000). The modern taxonomic classification of indica and japonica with rather distant relationship in botany has been proposed and applied in breeding and evolutionary studies by using grain shape, hairiness of hull, hairiness of leaf, and phenol and potassium hypochlorite reactions (Kato et al., 1928; Oka, 1958; Cheng et al., 1984). The significant correlation between SD and the classification index of indica and japonica, however, was not found in this case, and that the correlation coefficients between SD and grain shape, hairiness of hull, hairiness of leaf, and phenol and potassium hypochlorite reactions were as low as 0.26, 0.01, −0.21, −0.25 and 0.08, respectively (Qian et al., 2000). Super high-yielding rice, the next target of rice breeding in the 21st century, will be the hybrid rice in China. PHS in hybrid rice grain and seed production and male sterile line multiplication resulted in a heavy loss of grain yielding and degrading of rice quality
161 (Hu et al., 2003). So the control of SD is very important for controlling PHS in rice breeding. The QTL, CT339-G62 on chromosome 3 was consistent with those identified in other rice populations. This QTL may be desirable for MAS (Mackill & Ni, 2001) and gene cloning (Li et al., 2003) because it seems to have consistent effect across different genetic backgrounds. The QTL controlling SD identified in the present study should accelerate the breeding of new rice varieties with suitable SD.
Acknowledgement This study is supported by a grant to Longbiao Guo from the National Natural Science Foundation of China.
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