Crop Science 41:1240-1246 (2001)
© 2001 Crop Science Society of America
CELL BIOLOGY & MOLECULAR GENETICS
Comparison of Molecular Linkage Maps and Agronomic Trait Loci between DH and RIL Populations Derived from the Same Rice Cross
P. He,
J. Z. Li,
X. W. Zheng,
L. S. Shen,
C. F. Lu,
Y. Chen and
L. H. Zhu*
Institute of Genetics, Chinese Academy of Sciences, Beijing 100101, China
* Corresponding author (lhzhu{at}genetics.ac.cn)
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ABSTRACT
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Doubled haploid (DH) and recombinant inbred line (RIL) populations are two types of permanent populations for rice (Oryza sativa L.) breeding and genetic mapping. In this study, we report the comparison of molecular maps and mapped agronomic trait loci between DH and RIL populations derived from the same rice cross, ZYQ8 (indica) x JXI7 (japonica). We investigated six agronomic traits (days to heading, plant height, number of spikelets per panicle, number of grains per panicle, 1000-grain weight, and seed set percentage) and found that five of them did not show significant differences between the two populations. Restriction fragment length polymorphism (RFLP) and microsatellite markers were selected to construct two linkage maps of the DH and RIL populations. All the DNA markers except G39 showed the same linkage groups and orders between the two populations. The genetic distance per chromosome in the RIL population was shorter than that in the DH population, and the total genetic distance of genome in the RIL population (1465 cM) was 70.5% of that in the DH population (2079 cM). In the RIL population, 27.3% markers showed distorted segregation at P < 0.01 level, of which 90% markers favored indica alleles, while in the DH population, the skewed markers favoring indica and japonica alleles were in accordance with 1:1 ratio. Eight commonly distorted regions on chromosomes 1, 3, 4, 7, 8, 10, 11, and 12 were detected in both RIL and DH populations, of which seven skewed toward indica alleles and one toward japonica allele. Five of them were located near gametophytic gene loci (ga) and/or sterility gene loci (S). We also compared the quantitative trait locus (QTL) mapping results between the DH and RIL populations and found a number of similarities in the QTL locations between these two populations. So both RIL and DH populations are equally effective in rice breeding and genetic analysis.
Abbreviations: AFLP, amplified fragment length polymorphism • cM, centimorgan • DH, doubled haploid • LOD, logarithm of odds ratio • PCR, polymerase chain reaction • QTL, quantitative trait locus • RAPD, random amplified polymorphic DNA • RFLP, restriction fragment length polymorphism • RIL, recombinant inbred line • SSD, single seed descent
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INTRODUCTION
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SINCE 1988, when McCouch et al. reported the first molecular linkage map of rice, many linkage maps based on various rice populations have been constructed and widely used for mapping QTLs, positional cloning, and comparative genome research (Causse et al., 1994; Song et al., 1995; Gale and Devos, 1998; Harushima et al., 1998; He et al., 1998). Most of maps were independently constructed from either segregating F2 or backcross populations. These populations are highly heterozygous and cannot be propagated indefinitely through seed. Linkage maps based on DH or RIL populations are permanent and suitable for sustained genetic studies, especially for QTL identification. In rice, the DH populations can be quickly constructed via anther culture, while establishing a RIL population takes many years of continuous self-pollination. Some comparisons between DH and RIL populations have been made in maize, Zea mays L. (Mrigneux et al., 1993), wheat, Triticum aestivum L. (Henry et al., 1988), and rice (Courtois, 1993; Antonio et al., 1996). But, so far, few reports are available comparing DH and RIL populations from the same rice cross.
We have developed a rice DH population of 150 lines by anther culturing an F1 hybrid between indica ‘ZYQ8’ and japonica ‘JXl7’. The genetic linkage map contains more than 440 DNA markers, including RFLP, amplified fragment length polymorphism (AFLP), random amplified polymorphic DNA (RAPD), and microsatellite markers (Shen et al., 1998), and has been used to identify many QTLs controlling yield components, anther culturability, and grain quality (Lu et al., 1996; Liu et al., 1997; He et al., 1998, 1999). Recently, we established a RIL population of 107 lines derived from the same ZYQ8/JX17 cross by the single-seed-descent (SSD) procedure. One hundred fifty-four evenly distributed markers in the DH population map were used to construct the linkage map of the RIL population. In this study, we compared the linkage maps and mapped agronomic trait loci between these two permanent rice populations.
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MATERIAL AND METHODS
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Experimental Populations and Phenotypic Evaluations
The RIL population was derived from a cross between indica ‘ZYQ8 and japonica JX17 by SSD. One panicle was harvested from each individual ZYQ8/JX17 F2 plant and one seed from each panicle was chosen randomly and planted in the field to obtain F3 plants. This procedure was continued in the following generations until F8 plants were obtained. Approximately 50 seeds were collected from each F8 plant to produce F9 RIL. The plants were grown twice per year, at Beijing from May to September, and at Hainan from December to April. Beijing is located at 39°N (degree of northern latitude) and Hainan is at 18°N. Both locations had been used for growing rice many time and there was adequate insect, disease and weed control. The RIL population in this study included 107 lines. The doubled haploid (DH) population of 150 lines was described in a previous report (Lu et al., 1996).
The field experiment was conducted on the farm of the Institute of Genetics, Chinese Academy of Sciences, Beijing. For each line, two rows of 30 plants were planted. The parents were grown in one row each between every 10 lines as a control. Days to heading, plant height, number of spikelets per panicle, number of grains per panicle, 1000-grain weight, and seed set percentage were evaluated for each line on the basis of the average value of 10 individual plants. The days to heading was defined as the days from sowing to the main culm heading. The plant height was the distance from soil to the top of the plant. These two parameters were measured before harvest. After harvest, the spikelet and grain of panicle on main culm were counted as number of spikelets per panicle and number of grains per panicle. One thousand dry and mature seeds for each line were weighed as 1000-grain weight. Seed set percentage was defined as the ratio of filled spikelets relative to the total number of spikelets per panicle.
Molecular Map Construction
Rice genomic DNA was extracted from young leaves, and then digested with eight restriction endonucleases: BamHI, BglII, DraI, EcoRI, EcoRV, HindIII, ScaI, and XbaI. The restriction fragments were size separated, blotted, and hybridized to marker probes as described by McCouch et al. (1988). PCR amplification and primer sequences of microsatellites followed Chen et al. (1997). The linkage map was constructed with the software MAPMAKER/EXP ver. 3.0 (Lander et al., 1987; Lincoln et al., 1993a). Kosambi function was used to calculate the genetic distances between the markers and a LOD threshold of 3.0 was chosen. The graphical genotype of each line was established and the percentage of ZYQ8 genome was estimated by HYPERGENE (Young et al., 1989).
QTL Detection
Interval QTL mapping was carried out with the software Mapmaker/QTL Ver 1.1 (Lander et al., 1989; Lincoln et al., 1993b). We used a LOD threshold of 3.0 for declaring the presence of a putative QTL, and we considered a LOD score between 2.0 and 3.0 as suggestive of the presence of a putative QTL. The LOD peak of each significant QTL was considered as the QTL location in the linkage map. In addition, the additive effect and percentage of variation explained by an individual QTL were also estimated. The QTLs were named according to the suggestion of McCouch et al. (1997).
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RESULTS
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Distributions of Six Agronomic Traits in Two Populations
The approximately normal distributions of six agronomic traits: days to heading, plant height, number of spikelets per panicle, number of grains per panicle, 1000-grain weight and seed set percentage were observed in both DH and RIL populations (data not shown). The means and ranges of these traits in the two populations are listed in Table 1. Though the plants in the RIL population were significantly taller than those in the DH population, the other five traits did not show significant differences between the two populations. Days to heading and number of spikelets per panicle were similar to each other in the two populations, but they distributed in a wider range in the RIL population than in the DH population. The mean and range of 1000-grain weight in the RIL population were slightly lower than those in the DH population, while number of grains per panicle and seed set percentage in the RIL population were slightly higher than those in the DH population.
Comparison of Linkage Maps between Two Populations
Genetic Distance and Order of DNA Markers
On the basis of the same set of RFLP and microsatellite markers, two linkage maps of DH and RIL populations were constructed (Fig. 1). The genetic distance per chromosome and the total genetic distance of the genome are listed in Table 2. The distance of each chromosome in the RIL population was shorter than that in the DH population, and the total genetic distance in the RIL population was 70.5% of that in the DH population. Among 12 chromosomes, chromosomes 6 and 7 showed the least difference in genetic distances between two populations, and chromosome 9 showed the greatest difference, where the distance in the RIL population was about 50% of that in the DH population. All the DNA markers that were commonly mapped in the two populations displayed the same linkage groups and linkage orders except marker G39, which had been previously located to chromosome 1 in the DH population and was found on chromosome 2 in the RIL population.
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Fig. 1. Molecular linkage maps of rice ZYQ8/JX17 RIL and DH Populations. Map function is Kosambi function. The left chromosomes are based on the RIL population and the right chromosomes are based on the DH populations. Distorted segregation regions skewing to ZYQ8 are marked with down arrows and the regions skewing to JX17 are marked with up arrows (P < 0.05). Possible position of gametophyte loci (ga) and sterility loc (S) near commonly distorted segregation chromosomal regions in the two populations are indicted by italic and bold letters to the left of the chromosomes.
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Distorted Segregation
All of the DNA markers showing skewed segregation in the two populations are marked in Fig. 1. Among all the 154 markers, segregation deviating from the expected 1:1 ratio was determined based on a Chi-square test at P < 0.05 and P < 0.01 levels. In the RIL population, at P < 0.05 level, 75 markers (48.7%) showed distorted segregation, of which 68 markers skewed toward ZYQ8 alleles and 7 toward JX17 alleles. At P < 0.01 level, 42 markers (27.3%) showed distorted segregation, of which 38 markers favored ZYQ8 alleles and four favored JXI7 alleles. Thus, in the RIL population 90% of distorted segregation markers were toward indica alleles, and only 10% of them were toward japonica alleles. In the DH population, 37.1 and 18.2% of markers showed distorted segregation at P < 0.05 and P < 0.01 level, of which, 51% were toward ZYQ8 alleles and 49% toward JX17 alleles. This indicated that DH population reduced the occurrence of distorted segregation compared with RIL population.
Most markers with distorted segregation were comparable between the two populations. The skewed markers on chromosomes 1, 3, 7, 8, 10, 11, and 12 were toward indica alleles, while the markers in the middle of chromosome 4 were toward japonica alleles in both DH and RIL populations. Aside from these markers, there were no other commonly deviated segregation regions in the two populations. On chromosome 6, some markers were biased toward indica alleles in the DH population, while they were skewed toward japonica alleles in the RIL population. On chromosome 9, some markers were found skewed toward indica alleles and others toward japonica alleles in the RIL population, while none of them showed significant segregation distortion in the DH population.
Graphical Genotypes
The graphical genotypes of the RIL and DH lines were estimated by HYPERGENE software. The ZYQ8 genome ratio showed continuous distribution in the two populations (Fig. 2). In the DH population, the genome proportion of ZYQ8 ranged from 0.17 to 0.84, and the average was 0.497. This indicated that the genome ratios of ZYQ8 and JX17 were similar to each other, and they were randomly distributed in the DH population. However, in the RIL population, the genome proportion of ZYQ8 ranged from 0.02 to 0.99, and the average was 0.58, indicating that the ZYQ8 genome ratio was slightly higher than JX17 genome ratio in the RIL population.
QTL Mapping
Interval QTL mapping was carried out with the software MAPMAKER/QTL ver 1.1 (Lander et al., 1987; Lincoln et al., 1993a) for the six agronomic traits in the RIL population, and the results are shown in Table 3.
Two QTLs for days to heading, qHD-8 and qHD-12, were identified on chromosomes 8 and 12. The positive additive effects of them were from parent JX17. The QTL, qHD-8, was a major gene, explaining 35.2% of the total variation. Two QTLs, qPH-l and qPH-4, were found for plant height on chromosomes 1 and 4 with positive additive effects from JX17. The major QTL, qPH-l, explained 31.5% of the total variation. For number of spikelets per panicle, two QTLs, qSPN-4 and qSPN-6, were located on chromosomes 4 and 6. The JX17 allele of qSPN-4 and ZYQ8 allele of qSPN-6 increased the number of spikelets per panicle in the RIL population. For number of grains per panicle, only one QTL, qGN-4, was identified on chromosome 4, which was linked with qSPN-4. No QTL with a LOD threshold of more than 2.0 was detected for 1000-grain weight and seed set percentage. We previously used the DH population to detect the QTLs for these six agronomic traits in four locations: Beijing, Hangzhou, Hainan (Lu et al., 1996), and Chengdu (unpublished data, 1997). By comparing the QTL mapping results between the DH and RIL populations, we found a number of similarities in the QTL locations between these two populations. As for days to heading, a major gene (qHD-8) explaining more than 30% of the total variation was identified near marker RG885 on chromosome 8 in both populations, but the other QTL, qHD-12, was not detected in the DH population. Two QTLs for plant height, qPH-1 and qPH-4, in the RIL population, were also detected in the DH population, of which, qPH-1 was detected as a minor gene in Chengdu and qPH-4 was well replicated in both Hangzhou and Hainan. For number of spikelets per panicle, two QTLs, qSPN-4 and qSPN-6, were detected in all four locations in the DH population as well as in the RIL population. For number of grains per panicle, one QTL, qGN-4, was found in both populations, but the other QTL, qGN-6, was only detected in the DH population. As for 1000-grain weight, a number of minor loci were detected in the DH population, while no loci were detected in the RIL population. For seed set percentage, a few loci were mapped in the DH population, but no loci were found in the RIL population.
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DISCUSSION
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Distorted segregation can be found in a wide range of organisms and with almost any kind of genetic markers (Zamir et al., 1986). Wang et al. (1994) developed a linkage map of 127 RFLP markers based on a rice RIL population. Most of the markers were deviated toward indica alleles except six markers with at least 50% japonica alleles, and the overall average of indica genome was as high as 80% in the RIL population. In the present study, skewed segregation toward indica alleles was also observed in the RIL population, but the DH population reduced the occurrence of distorted segregation compared with the RIL population. Xu et al. (1997) compared chromosomal regions associated with distorted segregation markers in rice on the basis of six linkage maps including the present ZYQ8/JX17 DH population and a ZYQ8/JX17 F2 population also developed in our laboratory (Xu et al. 1993). They observed significant skewing toward indica alleles in backcross, RIL and F2 populations and found that eight chromosomal regions (chromosomes 1, 3, 4, 6, 7, 11, and 12) were located at or near previously reported gametophytic gene loci (ga) and/or sterility loci (S) (Kinoshita, 1991, 1993). In this study, eight commonly distorted regions on chromosomes 1, 3, 4, 7, 8, 10, 11, and 12 were detected in both RIL and DH populations, seven of which were toward indica alleles, and the other one toward japonica allele. Five of them were near ga or S genes, i.e., ga-9 on chromosome 1, ga-2 and ga-3 on chromosome 3, s-e-2, ga-6 and ga-10 on chromosome 4, ga-11 and S-7 on chromosome 7, and ga-13 on chromosome 12. So distortion in these regions might be due to ga or S genes.
Antonio et al. (1996) compared the genetic distance and order of DNA markers in five populations of rice derived from different crosses. They found that all DNA markers commonly mapped in the five populations showed the same linkage groups with conserved linkage order, and the genetic distance between markers among the different populations did not vary significantly on any of the 12 chromosomes. They pointed out that any major genetic information from a high density map can be expected to be approximately the same in the other crosses or populations. In this report, the two populations were derived from the same cross combination and, therefore, the mapping results from these two populations should be more comparable. We found uniform marker orders on all 12 chromosomes between the two populations, though most of the genetic distances between the markers in the RIL population were shorter than those in the DH population. We have constructed three molecular linkage maps from three different DH populations, each of which covered about 2000 cM (Li et al., 1996; Lu et al., 1996). They exceeded about 30% compared with Nipponbare/Kasalath map (1521.6 cM) (Harushima et al., 1998) and B8125/WL02/BS125 map (1491 cM) (Causse et al., 1994). These two maps' distances were near to the total genetic distance (1465 cM) of the ZYQ8/JX17 RIL map of the present study. DH populations are derived from male gametes through one meiosis, while RIL populations are from male and female gametes through many generations of selfing. Thus differences in the genetic distance between the DH and RIL populations may reflect differences in recombination rates between male and female gametes during meiosis.
QTLs for plant height, days to heading, and yield components have been widely mapped, but the results are not identical because of the different populations used (Lu et al., 1996; Li et al., 1997, Yano et al., 1997, Zhang et al., 1997). We planted ZYQ8/JX17 DH populations in four different locations to study QTL x environment interaction (Lu et al., 1996). The QTL mapping results indicated that number of spikelets per panicle and number of grains per panicle were less influenced by environments than plant height and days to heading. The same conclusion was obtained in the RIL population of the present study. In addition, the QTLs for these traits can be detected repeatedly in the two populations. On the basis of these detected common QTLs, the establishment of near-isogenic lines for these QTLs is in progress in our laboratory.
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ACKNOWLEDGMENTS
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This study was jointly supported by the Rockefeller Foundation and the National High-Tech Research Program of China. All the RFLP markers in this study were kindly provided by Dr. S.D. Tanksley and Dr. S.R. McCouch from Cornell University and the Rice Genome Research Program (RGP) of Japan. We thank Drs. R. Warren and Y.B. Xu for valuable advice and comments.
Received for publication May 15, 2000.
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TOP
ABSTRACT
INTRODUCTION
