Copyright  2001 by the Genetics Society of America

Overdominant Epistatic Loci Are the Primary Genetic Basis of Inbreeding
Depression and Heterosis in Rice. II. Grain Yield Components
L. J. Luo,* Z.-K. Li,†,‡ H. W. Mei,* Q. Y. Shu,§ R. Tabien,† D. B. Zhong,* C. S. Ying,*
J. W. Stansel,‡ G. S. Khush‡ and A. H. Paterson†,**

Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas 77843, *China National Rice Research Institute,
310006 Hangzhou, China, ‡Plant Breeding, Genetics, and Biochemistry Division, International Rice Research Institute, Metro Manila, The
Philippines, §Department of Agronomy, Zhejiang Agricultural University, 310029 Hangzhou, China and **Applied Genetic Technology Center,
Departments of Crop and Soil Sciences, Botany, and Genetics, University of Georgia, Athens, Georgia 30602

Manuscript received August 25, 2000
Accepted for publication May 14, 2001
ABSTRACT
The genetic basis underlying inbreeding depression and heterosis for three grain yield components of
rice was investigated in five interrelated mapping populations using a complete RFLP linkage map,
replicated phenotyping, and the mixed model approach. The populations included 254 F10 recombinant
inbred lines (RILs) derived from a cross between Lemont ( japonica) and Teqing (indica), two backcross
(BC) and two testcross populations derived from crosses between the RILs and the parents plus two testers
(Zhong413 and IR64). For the yield components, the RILs showed significant inbreeding depression and
hybrid breakdown, and the BC and testcross populations showed high levels of heterosis. The average
performance of the BC or testcross hybrids was largely determined by heterosis. The inbreeding depression
values of individual RILs were negatively associated with the heterosis measurements of the BC or testcross
hybrids. We identified many epistatic QTL pairs and a few main-effect QTL responsible for ⬎65% of the
phenotypic variation of the yield components in each of the populations. Most epistasis occurred between
complementary loci, suggesting that grain yield components were associated more with multilocus genotypes than with specific alleles at individual loci. Overdominance was also an important property of most
loci associated with heterosis, particularly for panicles per plant and grains per panicle. Two independent
groups of genes appeared to affect grain weight: one showing primarily nonadditive gene action explained
62.1% of the heterotic variation of the trait, and the other exhibiting only additive gene action accounted
for 28.1% of the total trait variation of the F1 mean values. We found no evidence suggesting that pseudooverdominance from the repulsive linkage of completely or partially dominant QTL for yield components
resulted in the overdominant QTL for grain yield. Pronounced overdominance resulting from epistasis
expressed by multilocus genotypes appeared to explain the long-standing dilemma of how inbreeding
depression could arise from overdominant genes.

I

NBREEDING depression, the overall decline in fitness-related traits arising from increased homozygosity, and heterosis, the superiority of F1 hybrids relative
to parental performance, are fundamentally concerned
with outbreeding and inbreeding. The negative effect
of inbreeding and the positive effect of outbreeding
have been known since ancient civilization (Goldman
1998; Filho 1999). Inbreeding depression and heterosis
are considered two aspects of the same phenomenon
(Falconer 1981; Mather and Jinks 1982). Heterosis
is the opposite of inbreeding depression in the sense
that the vigor lost as a consequence of inbreeding is
recovered by crossing (Filho 1999). In agriculture, the
use of heterosis in different crop plants and animals
has achieved great success and is considered essential to
meeting the world’s food needs (Duvick 1999; Phillips
1999).
Corresponding author: Zhi-Kang Li, Plant Breeding, Genetics, and
Biochemistry Division, International Rice Research Institute, DAPO
7777, Metro Manila, The Philippines. E-mail: z.li@cgiar.org
Genetics 158: 1755–1771 (August 2001)

Despite its tremendous success in plant and animal
breeding, the genetic basis of heterosis remains uncertain. Theories include dominance (Bruce 1910), overdominance (Shull 1908; East 1936), and certain types
of epistasis (Stuber et al. 1973, 1992). In all cases, inbreeding depression is considered due to segregation
and expression of deleterious recessive alleles in the
homozygous state in inbred progenies (Allard 1960;
Simmonds 1979; Filho 1999). Results from recent quantitative trait locus (QTL) mapping studies in major crops
have done little to alleviate the controversy regarding
the genetic basis of heterosis. Stuber et al. (1992) reported that overdominance was observed at most QTL
for grain yield and components in two maize backcross
F3 (BCF3) hybrid populations. However, Xiao et al.
(1994) concluded that dominance is the major genetic
basis of heterosis of most QTL segregating in two rice
BCF1 populations. Li et al. (1997a,b) reported that hybrid breakdown (part of inbreeding depression) in an
intersubspecific F4 population was largely due to additive epistatic loci, which implies epistasis as a genetic

RESULTS Inbreeding depression and heterosis: Table 2 shows the summary statistics for the yield components of the parents. and a check hybrid. However. 2001). each consisting of one row of a RIL and two rows of testcross F1 hybrids (the RIL ⫻ the testers. grains per panicle. two BCF1 populations. F1 (Lemont ⫻ Teqing). was constructed using MAPMAKER/EXP version 3. 2001). RILs. two separate experiments were conducted at two locations. were used. were planted in the seedling nursery on May 25. Luo et al. and testers was extracted from freshly harvested leaves of 25-day-old seedlings grown in the greenhouse at Texas A&M University. with all QTL fixed in the model to control the background genetic variation. basis of heterosis. In this article. each consisting of a single row of the female RIL and the two BC1F1 hybrids (the RIL ⫻ Lemont and Teqing). HMP. MATERIALS AND METHODS Development of the experimental populations: A set of 254 F10 recombination inbred lines (RILs) derived from a cross between Lemont ( japonica) and Teqing (indica). HC ⫽ 100 ⫻ (F1 ⫺ Shanyou63)/Shanyou63.1992). SAS PROC GLM (SAS Institute 1996) was used to test the differences among the RILs and the BC/testcross hybrids. were developed and used in this study (Li et al. 1. A complete linkage map with 182 markers spanning 1918. as well as the . parental lines. genetic parameters (effects and test statistics) associated with significant main-effect and epistatic QTL were simultaneously estimated at the positions of respective LOD peaks in individual putative QTL regions (each putative QTL region covered two marker intervals) using the model and the restricted maximum likelihood estimation method (Wang et al. QTL mapping was carried out in three steps using the computer software. Zhong 413. was evaluated for the RILs.005 for main-effect QTL and P ⱕ 0. this possibility was examined by exploring the relative importance of main-effect QTL and digenic epistatic loci associated with inbreeding depression and heterosis of the three grain yield components in the five related mapping populations. all putative main-effect and epistatic QTL were identified using interval mapping in putative QTL regions identified in the first step. The field arrangement in CNRRI was the same as the ZAU experiment except that three replications were used. and Shanyou63 were also included in each replication. 1996. Teqing.0 (Lincoln et al. parents.0 were used for interval mapping of main-effect and epistatic QTL in each of the mapping populations. Recently. Data analyses: The original data of the three yield components and the square-root-transformed data for GP of the RI. three representative plants from the middle of each row plot were sampled and dried in an oven. Z413. where BP and Shanyou63 were the better parent and the check hybrid. as described previously (Li et al. One of the testers. 2001). the RILs. In the CNRRI experiment. In addition. The threshold was 0. including 192 Z413 test F1 hybrids (the RILs ⫻ Zhong 413) and 187 IR64 test F1 hybrids (the RILs ⫻ IR64). in grams). and the mean values of individual BC and testcross F1 hybrids for the three traits were used to identify QTL contributing to heterosis.1756 L. First. since yield per plant was the product of its three direct components. The mixed linear model and the computer software QTLMAPPER v. For mapping main-effect and epistatic QTL. is an indica cultivar developed in IRRI. Yu et al. Finally. 2001). Z413 and IR64). Teqing. panicles per plant. the same three-row plots. Genotyping and RFLP map construction: Genomic DNA of the RILs. and two testcross F1 populations. including 172 LTBCF1 hybrids (RILs ⫻ Lemont) and 177 TQBCF1 hybrids (RILs ⫻ Teqing). 1999. two BC1F1 populations. Li et al. as described previously (Wang et al. Restriction fragment length polymorphism (RFLP) mapping was conducted using published procedures (Li et al. data from each of the mapping populations were analyzed separately. six check plots consisting of Lemont. and two testcross populations. 1995) and 179 well-distributed RFLP markers from Cornell University and the Japanese Rice Genome Research Program. significant markers were identified across the genome using stepwise regression analyses based on single marker genotypes for putative main-effect QTL and based on all possible pairwise marker pairs for epistatic QTL with a threshold of P ⱕ 0. effective panicles per plant (PP).7 cM and covering 12 rice chromosomes with an average interval of 11. F1 (Lemont ⫻ Teqing). IR64. J. C (apiculus color) and gl-1 (glabrous leaf) in the field. and grain weight. 1999).3 cM between markers. Zhejiang Agricultural University (ZAU) and China National Rice Research Institute (CNRRI) in 1996. and testcross hybrid populations were used in the data analyses with each population analyzed separately. Shanyou63 (the most widely grown commercial hybrid cultivar in China). 2001). Four check plots consisting of Lemont. The RILs were also evaluated for two morphological markers. The plots were arranged in a randomized complete block design with two replications. (1997) also reported that additive epistasis was largely responsible for the grain yield and its components in an F3 population of rice. it remains unclear if the observed epistasis and apparent overdominance of the yield QTL actually resulted from the multiplicative actions of partially or completely dominant QTL affecting yield components. At the maturity stage. respectively. Each row within a plot consisted of 15 plants with a spacing of 20 cm between plants within each row and 35 cm between rows. and the competitive heterosis. HBP ⫽ 100 ⫻ (F1 ⫺ BP)/BP. and the two BC1F1 populations (LTBCF1s and TQBCF1s). F1.005. the reaction to phenol (Ph). IR64. An additional marker. F1 plants. Equations for calculating values of hybrid breakdown (a component of inbreeding depression) of individual RILs and the midparental heterosis for the three traits of individual BC/testcross hybrids are listed in Table 1. parents. 1999. Phenotypic evaluation: As described previously (Li et al. In the ZAU experiment. BCF1. and Shanyou63 were randomly arranged in each replication. The 25-day-old seedlings were transplanted into threerow plots. IR64 is a popular restorer line for cytoplasmic male sterility rice lines and the most widely grown variety in South and Southeast Asia.001 for epistatic QTL. and 1000-grain weight (GW. In addition. and testers. Each sampled plant was evaluated for grain yield and three major yield components. Then. we reported that epistasis and overdominance are the major genetic bases of inbreeding depression and heterosis for grain yield and biomass in five related rice mapping populations (Li et al. The mean midparental heterosis. two other relative heterosis measurements were calculated as follows: the better parental heterosis. filled grains per panicle (GP). The mean values of individual RILs for the three yield components and the genotypic data at the 182 RFLP loci of the RILs were used as input data to identify QTL showing additive gene action. is a widely compatible restorer line developed in China and the other.

1%) and 39.5 (65.6 (90.2%) for PP. the mean deviation of the RILs from the midparental values was ⫺0.2 for GP. respectively (Table 2 and Figure 1). and GW than Lemont (japonica) in both experiments. In the CNRRI experiment.8 g for GW. In the CNRRI experiment.7 (137. In the ZAU experiment.7 (25.0%) and 2. 99. and 2.8 (⫺7. and GW values of the F1 plants were 9. The top 20 high-yielding hybrids in the LTBCF1 population had a mean heterosis of 5. b F1 are mean trait values of individual BC or testcross hybrids while RIL is the corresponding female RIL parent for each of the BC or testcross hybrids. HC. but none for GP. 42. their heterosis.4 g (1.1 g (8.5%) for PP.7%) for GP. estimated hybrid breakdown (HB) and the HMP of the BCF1 and testcross F1 hybrids. The top 20 high-yielding hybrids in the IR64F1 population had a mean heterosis of 9.0 for GP.8%) for GP. In the CNRRI experiment. and F1 performance: Table 3 shows the correlation coefficients between the mean values of individual F1 hybrids.8%) and 2.9 (83.0%) for GW. respectively.8 (28. and 0. respectively.1%) for GW. and ⫺1.5 and 24. GP.1 (100.2 (86. GP. 123. Hybrid breakdown of the RILs: In both ZAU and CNRRI experiments. of the top 20 high-yielding hybrids of the Z413F1 and IR64CF1 populations was –0. the two BCF1 populations showed the same levels of heterosis for PP and GP. ⫺27. 107. the mean hybrid breakdown of the RI population was ⫺0. where MP ⫽ (RIL ⫹ Z413)/2 HMP ⫽ F1 – MP.2 (64. was two for PP. and GW was 2.1 (34. 142.1 (⫺74. Lemont (LT) and Teqing (TQ).6 (36. ⫺13.5%) ranging from ⫺12. The heterosis values were 2.9 (⫺12.6%). GP. and 3.9 (58.8 and 15. and 26. 157. GP.0 (9. respectively.3 (12.7%) for GW. Heterosis in the BC and testcross F1 populations: Significant levels of heterosis for PP. The male parent. respectively. Teqing (indica).4 (6. most F1 hybrids showed highly significant positive heterosis. the mean values of the LTBCF1 and TQBCF1 populations were 8.0%) for GW. and 24.6 for PP. and 5. Six RILs had significantly higher mean values than Teqing for PP and GW.9 g in the ZAU experiment.4%) for PP.7 (45.7 (24. but not for GW (Table 2).9%) for PP.9 for PP. The top 20 high-yielding hybrids in the TQBCF1 population had a mean heterosis of 6.3 (⫺1. and 24.5%) for GW.3%). 50.3 (86. and 0.0%) in CNRRI.6%) and 46.1%) for GP.4%) for GP.7 and 9. and 1. and 1. and ⫺0.3%) and 4.1 (7.1 (16. 128. Their mean HMP values were 2.7 (11.8 (⫺7.9%) for PP. Teqing.8 (165.6%) and 3. while Z413F1s and IR64F1s are two testcross F1 populations obtained by crossing the RILs with the testers Zhong 413 (Z413) and IR64. respectively.2 (117. respectively.3 (31.7%) for PP.9 g (3. The PP. and GW were observed in the BCF1 and testcross hybrid populations and heterosis values of individual BC/testcross F1 hybrids varied considerably (Table 2 and Figure 1). The midparental heterosis of the F1 plants for PP.1%) to 11.0%) for PP.2 (43.2%) for GP. and 24. and 2.7. had significantly greater trait values for PP. and 11. 10. Many hybrids showed significant negative heterosis for the three yield components.1%) for GW.8 g in the CNRRI experiment.4%) for GP.9.2 (⫺24.5%) to 6. and 1. respectively.5%) for GW. The relationships between the mean trait values of RILs.8. In ZAU. and the mean val- . and nine for GW. respectively. 89 (78.6 (42. 56. Within each of the populations.0%) ranging from ⫺63.4%) for PP. respectively. significant reductions of the RILs for PP and GP were observed as a result of hybrid breakdown.4 g for GW. In the ZAU experiment. but LTBCF1s exhibited greater mean heterosis for GW than TQBCF1s. II 1757 TABLE 1 Equations for calculating HB of the Lemont/Teqing RILs and the midparental heterosis (HMP) of the two BCF1 and two testcross F1 populations Populationa RILs LTBCF1 TQBCF1 Z413BCF1 IR64BCF1 N Equationsb 254 172 177 192 187 HB ⫽ RIL – MP.8 and 129.4%) and 3. individual F1 hybrids varied considerably in their mean values and heterosis measurements (Figure 1).8 (⫺95.5 (51. The top 20% high-yielding hybrids in the Z413F1 population had a mean heterosis of 7.1 (0.7%) for PP. particularly for GW.6%) for GW in the LTBCF1 and TQBCF1 populations.5 (⫺16. where MP ⫽ (RIL ⫹ Lemont)/2 HMP ⫽ F1 – MP.9 (12.2%) and 0. and 5.9 (16.5 and 134.8%). where MP ⫽ (Lemont ⫹ Teqing)/2 HMP ⫽ F1 – MP. the IR64F1 population showed a much greater level of heterosis than the Z413F1 population for all three traits.7 (2.6%) ranging from ⫺6. the mean values of the Z413F1 and IR64F1 populations were 13.Inbreeding Depression and Heterosis in Rice. 201.9 (197. where MP ⫽ (RIL ⫹ Teqing)/2 HMP ⫽ F1 – MP.7%). respectively. The competitive heterosis. respectively.1%) for GP. two for GP.0%) and 57.8%) in ZAU. heterosis. The number of RILs having significantly higher values than the better parent. For PP and GP.8 (23.8 (45.4%) for GP.6 (38. 73.0 and 25.8%) for GW.7%) to 85.6.5%) for GP.4 (5. where MP ⫽ (RIL ⫹ IR64)/2 a LTBCF1s and TQBCF1s are two BCF1 populations obtained by crossing the RILs with the parents.

34.7 25.5 ⫺42.9 ⫺12.862 for GP.2 89.3 25.4 ⵑ 169.0 ⫺5. respectively.8 49.851. and 34. and 0.6 ⵑ 106. The mean values of the RILs and heterosis of the BC/ testcross F1 hybrids for all three traits were distributed in opposite directions around the midparental value (at the zero point) with varied degrees of overlapping in different populations (Figure 1).2 2.0 1.0 18.3 13. and IR64F1 populations were 21.0 49. TQBCF1. and GW to grain yield: All three yield components contributed significantly to the grain yield per plant in all five populations.0.3 5.6 a 2.7 24.7 3.0 – 5. 54.7 7. GP.1 21.1 ⫺8. Luo et al.8 14. 0. The mean trait values of individual RILs were negatively correlated (P ⬍ 0.0 4.2 1. 0.1 12.7 2. 11.930.8 2.9.6 15.6 9.8 21.5 50.9 0.1 38.4 ⫺44. and GW in the ZAU experiment.2.9 ⫺6.0 3.7 166.1 10. respectively (P ⬍ 0.7 31.3 1.0 73. 9. TQBCF1.6 12.4% for PP.0001) with their heterosis values in all BC and testcross populations (Table 3).9 ⵑ 181.2 ⫺3.4 6.6 17.0 16.1 25.0 126. ⫺0.4.5 14.6 – 77. The mean trait values of individual BC and testcross hybrids for PP.2 201.9 29.2.5 1.4 24.0001).0 27. g) Mean SD ⵑ ⵑ ⵑ ⵑ ⵑ ⵑ 22.6 1.5 9. However.5 134.2 ⫺0.4% for GP. This nega- tive association between the mean trait values of the RILs and the heterosis of their BC/testcross hybrids was stronger for PP (r ⫽ ⫺0. and IR64F1 populations was 0. and 7.7 HB ⫽ RIL – MP.5 ⵑ 199.4 34. 0. 66.1 1.363.5 29.5 14. For the RILs.0 26.4 ⵑ 234.7 2.31.2 3. GP.4 9. ⫺0.7 2.5 179.1.5 2.4 ⵑ 155.3 10. 0.9 4.9 ⫺27.2 83.3 9.7 2.5 2.5 2.5 107.9 4.5 18.0 8.2 2.3 ⫺5. the mean F1 values of GW in LTBCF1.3 5.9 64. and 10.8 Zhejiang Agricultural University 59.1.5 11.6 ⫺1.27.6 0.3 31.4 2.9 8. Z413F1. ues of their maternal RILs for the yield components. Regression analyses indicated that the contributions (partial R 2) to the total variances of the grain yield in the LTBCF1.1 21.290.2 ⵑ 16.3 7.005) was observed between PP and GW in the CNRRI experi- .143.1 2.2% for GW. and IR64F1 populations was positively associated with the mean trait values of the RILs with determination coefficients of 0.265.9% for PP. 0.915 for PP.5 37.5%.4.9 2.6 12.0 4.6 3.951.7 85.0 2. respectively.803. Z413F1.0 2.6 34.6 8. and ⫺0.0 142.4 26.9 15.1 ⵑ 85.9 ⵑ 283.2 2. and 0. There was no correlation between the mean trait values of the RILs and their F1 performance of BC or testcross hybrids for PP and GP.9 1.6 1.758.42.5 2.2 38.4 52.8 ⵑ 27. 0.812 for GW. 0.6 2.8 42.7 2.21.3 ⫺5.2 39. 24.8 2. and 0.8 ⫺13.2 9.8 1.7.5 ⫺84.8 2.0 48. Z413F1.9 ⵑ 25.1758 L.383. and 49.4 2. GP.586.3 ⫺3.0 ⫺12.2 21.3% in the CNRRI experiment. ⫺0.2 13.4 29.5 11.7 ⵑ ⵑ ⵑ ⵑ ⵑ ⵑ 31.2 27.9 1.6 13. The contributions of PP.0 70.7 ⫺10.9 3. and 0.890.247) than for GP (⫺0.367) and GW (⫺0.7 8.8 ⫺63. and GW were largely determined by the levels of heterosis.1 7.7 30.838.6 23.1 ⵑ 11.6.5 26.2 1. 55. ⫺0.4 ⵑ 276.0 2.4 83.0 ⫺9. 71.8 27. TABLE 2 Summary statistics on inbreeding depression of the Lemont/Teqing RILs and the midparental heterosis (HMP) of two backcross F1 (RILs ⫻ parents) and two testcross F1 populations (RILs ⫻ two testers.9 2. Z413F1. and ⫺0. TQBCF1. Z413 and IR64) Panicles per plant (PP) Mean SD Lemont (LT) Teqing (TQ) F1 (LT ⫻ TQ) HMP CK (SY63) LTBCF1 (LTBC) HMP TQBCF1 (TQBC) HMP RILs HBa 6. TQBCF1. P ⫽ 0. and 13.2 109. and 0.5 6.9 ⫺104. and 7.6 157.0 20.68 Range 20. For the RILs.838.5 0.2 ⵑ 191.2 40.1 2.5 24.359.1. and ⫺0. the partial R 2 was 31.2 34.0 1.5 Range Grains per panicle (GP) Mean SD Range 1000-grain weight (GW.9 15.3 ⫺6.0 24.6%.1 2.8 9. ⫺0.9 24.5 ⫺21.937.2 1.4 0.8 1. 0.7 2. Correlation between the traits was weak and inconsistent across the populations and experiments.4 ⵑ 16.4 20.1 1.292.6 4. a weak positive correlation (r ⫽ 0.5 China National Rice Research Institute 59.5 Lemont (LT) Teqing (TQ) F1 (LT ⫻ TQ) HMP CK (SY63) Z413 IR64 Z413F1 (Z413F1) HMP IR64F1 (IR64F1) HMP RILs HB 9.1 ⵑ 233.3 6.5 129.8 2.0 ⫺0. and IR64F1 populations.6 2.8 1.5 0.272) in the LTBCF1.7 15.489. J. 60.7 2.34. ⫺0.5 8.5 ⵑ ⵑ ⵑ ⵑ ⵑ ⵑ 34.3 ⫺0. 0. where HB is hybrid breakdown and MP ⫽ (Lemont ⫹ Teqing)/2. The correlation between the F1 mean values and HMP in the LTBCF1. and 37.

P ⫽ 0.0%. ment. PP: Three main-effect QTL were detected in the RILs (one in ZAU and two in CNRRI) and mapped to chromosomes 3 and 4.8% for PP.2% for GW. 3. ranging from 0 to 15. P ⫽ 0. ranging from 11. five main-effect QTL were identified in the BC and testcross populations.7% of the total variation. II 1759 Figure 1.20. P ⬍ 0.3%.—Frequency distribution of hybrid breakdown (HB ⫽ RILs ⫺ MP) of the Lemont/Teqing RILs and the midparental heterosis (HMP) for three yield components in the two backcross and two testcross F1 populations. Main-effect QTL associated with the mean trait values of the RILs and heterosis of the BC/testcross F1 hybrids: Table 4 shows 30 main-effect QTL affecting the three yield components identified in the RILs and the BC/ testcross F1 populations.31.21.0002) was present between PP and GP in the ZAU experiment. but PP was negatively correlated with GP (r ⫽ ⫺0. ranging from 0 to 32.Inbreeding Depression and Heterosis in Rice.008) in the IR64F1 population.4%.01) was present between PP and GW.3 and explained 18. but was much stronger in the LTBCF1s (r ⫽ ⫺0.1% for GP. and 9. On average. The QTL on chromosome 4 was detected with a large LOD score of 10.22. . In the Z413F1 population. In addition. The Teqing allele at all three QTL increased the panicle number.0001) than in the LTBCF1s (r ⫽ ⫺0. but a weak negative correlation (r ⫽ ⫺0. P ⫽ 0. 20. respectively). which were mapped to chromosomes 1. a weak positive correlation (r ⫽ 0.0 to 26. these main-effect QTL explained a small portion of the total phenotypic variance in each of the populations (11. P ⫽ 0.59. Negative correlation between PP and GP was observed in the two BCF1 populations.01).

and 12.006 0. 4. These QTL were mapped to chromosomes 3. which explained the majority of the total phenotypic variances for the yield components (36.116 0. 37.890 0. The only additive QTL was detected on chromosome 1 in the TQBCF1.878 0.058 0.866 0.074 L. GW: Three main-effect QTL affecting GW were identified in the RILs (one in ZAU and two in CNRRI) and mapped to chromosomes 1. Five additional maineffect QTL were identified in the two BC and one testcross (Z413F1) populations.862 0.6 and 49.147 ⫺0.247 0. The dominance effects at three QTL on the chromosomes 1. Six detected in ZAU and 5 in CNRRI explained 36.5% for GW) in the CNRRI and ZAU experiments. and 10 caused increased GW while another QTL on chromosome 10 resulted in reduced GW.645 0.586 0. Epistatic loci associated with hybrid breakdown in the RILs and heterosis in F1 populations: Table 5 shows 35 digenic epistatic QTL pairs associated with hybrid breakdown of the RILs.344 ⫺0.4% for GP. two (between C225c and G2132a on chromosome 8 and between RG1094f and C16 on chromosome 10) were additive as they were detectable only by the F1 mean values.005 ⫺0. Luo et al.0 and 51.758 0.084 ⫺0. and 7.153 0.340 0.027 0. The other four QTL appeared to be overdominant.2% for GP. J. and 49.792 0. 3.838 0. IR64F1 1760 4. GP: Four main-effect QTL affecting GP (one in ZAU and three in CNRRI) were identified in the RILs and mapped to chromosomes 1.359 0.6 and 45.930 0.421 0.915 0.132 ⫺0. Two of the five QTL (chromosomes 4 and 7) were additive. Of these. and 9.367 0. The remaining 8 QTL appeared to be overdominant since the QTL effects estimated from heterosis values were equal to or greater than their effects estimated from F1 mean values.073 0. while the other three (chromosomes 1.143 0.702 0.066 0. 11.851 0.292 0. 73 pairs of epistatic QTL affecting the mean performance and heterosis in the BC/testcross F1 populations were identified.079 0.951 0. 6. 4.838 0.272 0.743 0.575 Z413F1 TQBCF1 TQBCF1 Z413F1 IR64F1 LTBCF1 Between HB and HMP Between HMP and F1 mean Phenotypic correlation (r) and determination coefficients (R ) for grain yield components between HB of the Lemont/Teqing RILs and the midparental heterosis (HMP) in the two BCF1 and two testcross F1 populations 0.089 0.177 0.072 Z413F1 TQBCF1 LTBCF1 Between HB and F1 mean IR64F1 LTBCF1 2 TABLE 3 ⫺0. The Teqing allele at all three QTL increased GW. On average.812 0. respectively.003 0. 57.020 ⫺0.134 ⫺0.⫺0. These three QTL had dominance effects for increased panicle number.032 0. In addition.097 GW GP PP r R2 r R2 r R2 ⫺0. these epistatic QTL explained significant portions of the total phenotypic variances for the traits (48.937 0. Eleven main-effect QTL affecting F1 mean values and/or heterosis were detected in the BC or testcross F1 populations.061 ⫺0. and 6) appeared to be overdominant as their effects estimated from heterosis values were equal to or greater than those estimated from F1 mean values.0% for PP. respectively.363 0.268 0. Four of the epistatic QTL effects were positive and the remaining seven were negative.024 0. and 12) had significant main effects .070 ⫺0.129 0.838 0. The Teqing allele at all QTL increased GP.178 0. 3. Three of the epistatic QTL (on chromosomes 7.265 0.1% for GW) in the BC/testcross F1 populations (Tables 6–8). Epistatic QTL affecting hybrid breakdown of the RILs: Eleven pairs of epistatic QTL associated with PP of the RILs were identified.290 0.659 0.489 0.8% for PP. and 10.0% of the total phenotypic variation for PP in the two locations.383 0. with the Teqing allele associated with increased GW. 6. 6.004 0. 8.803 0.905 0.164 0. 5. and 43.239 ⫺0. One QTL (between G103b and RZ698 on chromosome 9) detected in the LTBCF1s appeared to be dominant. 9.085 ⫺0.724 0.703 0.0 and 51.311 0.008 0.

53 0.66 0.50 0.42 ⫺1.ZAU CNRRI CNRRI ZAU ZAU ZAU CNRRI CNRRI ZAU CNRRI CNRRI CNRRI ZAU ZAU ZAU ZAU CNRRI CNRRI CNRRI CNRRI CNRRI CNRRI CNRRI ZAU CNRRI CNRRI ZAU ZAU ZAU ZAU CNRRI RILs RILs RILs TQBCF1 TQBCF1 TQBCF1 Z413F1 Z413F1 RILs RILs RILs RILs LTBCF1 TQBCF1 TQBCF1 TQBCF1 Z413F1 Z413F1 IR64F1 IR64F1 IR64F1 IR64F1 IR64F1 RI RI RI LTBCF1 LTBCF1 TQBCF1 TQBCF1 Z413F1 GW GW GW GW GW GW GW GW GP GP GP GP GP GP GP GP GP GP GP GP GP GP GP PP PP PP PP PP PP PP PP Traits 10 1 5 11 10 10 1 4 1 3 6 9 9 6 9 10 3 4 3 6 8 9 12 3 3 4 1 7 6 3 4 Chromosome G1084–RZ400 CDO118–CDO455 R569a–RG13 RZ781–C975 G89–G1084 RG561–C223 RG236–RZ801 RZ590–RG214 RZ14–C944b G249–RG418 RG653–RZ508 G103b–RZ698 G103b–RZ698 C235a–G294d RG451–RZ404 RG1094f–C16 G249–RG418 Ph–G379 C515–RG348a G1314b–HHU37 C225c–G2132a CDO395–CDO1081 RG901–G402 RG482–CDO795a C515–RG348a Ph–G379 CDO118–CDO455 RG678–G20 RG653–RZ508 RG341b–C74a Ph–G379 Marker interval 2.24 2.5 8.16 4. the additive and dominance effects (a ⫹ d) from the F1 mean values.71 0.62 ⫺0.01 ⫺0.9 R2 In the RI population.70 ⫺0.16 6.1 5.5 5.0 8.8 9.52 3.54 0.53 3.63 ⫺0.98 2. QTL effects were associated with the Lemont allele (the effect due to substitution of the Teqing allele by the Lemont allele).10 ⫺0.82 0.85 5. The genetic expectation of the QTL effect is the additive gene effect (a) when estimated from the RILs.12 0.32 4.26 LOD R2 7.62 3.9 10.49 0.56 ⫺0. and heterosis (HMP) in their BCF1 and testcross F1 populations in the ZAU and CNRRI experiments TABLE 4 Inbreeding Depression and Heterosis in Rice.28 5.67 2.5 14.9 18.11 2.58 ⫺0.3 13.18 4.47 2.17 16.61 0.24 1.6 11.75 1. grains/panicle (GP).22 4.42 6.75 3.1 7.1 15.1 14.1 5.73 3.97 ⫺0.36 3.13 LOD F1 1.15 0.0 7. a Location Population RILs Main-effect QTL associated with panicles/plant (PP).67 10.67 4.1 Effect ⫺0.41 0.2 ⫺1.6 11. II 1761 .00 1.7 5.46 0.93 3. In the BC populations. and 1000-grain weight (GW) in the Lemont/Teqing RILs.88 3.8 14.01 4.8 9.7 12.85 Effect 4. QTL effects for F1 and heterosis were estimated by the difference between the heterozygote (tester/Lemont) and the heterozygote (tester/Teqing).70 4.2 9.77 6.02 5.5 0. and the dominance effect (d) from HMP values in the BC populations.87 14.3 7.49 3.2 6.43 0.9 8.7 14.11 2.48 0.64 3.91 0.8 12.59 12.4 6. In the testcross populations.76 Effect 4.89 3.27 ⫺0.21 ⫺1.29 ⫺0.3 R2 4.84 2.2 6.5 6.33 0.80 ⫺0.55 10.3 12.32 5.43 LOD HMP 5.0 5.1 8.75 3.2 0.37 ⫺0.91 4.88 0.3 6.29 ⫺0.6 0.55 2.3 15.75 ⫺0. QTL effects for F1 and HMP were estimated by the difference between the heterozygote and the homozygote.58 0.

46*** 0.85*** ⫺0.98 4.59 5.2 11.0001.75*** ⫺0.93 2.68*** 1. arising from the substitution of the Lemont allele by the Teqing allele.83*** ai ⫺0.14 4.6 11.57 4.0 9.10*** ⫺0.45*** ⫺0. grains/panicle (GP).7 8.59 6.6 6.4 7.64 8.9 8.2 6.1 8.1 6.18 3.34 LOD ⫺0. *** Significance levels of P ⬍ 0. * Significance levels of P ⬍ 0.9 14.8 6.49** 0.58*** 0.69*** ⫺0.07 5.89 3.37*** 0. R 2 is the proportion of the total phenotypic variation explained by the aaij.95 6.3 5.45 5.31 6.07 3. as defined by Mather and Jinks (1982).0 7.59 3.7 10. Trait Location TABLE 5 Digenic epistatic QTL affecting hybrid breakdown of grain yield components — panicles/plant (PP).37* 0.28*** ⫺1.6 5.80*** ⫺0.81*** ⫺0.81*** ⫺0.60*** 0.20 3.53 4.60** aj QTL effect 6.3 9.74 5. and 1000-grain weight (GW) of the Teqing/Lemont recombinant inbred population in two environments 1762 L.94*** 0.PP PP PP PP PP PP PP PP PP PP PP GP GP GP GP GP GP GP GP GP GP GP GP GW GW GW GW GW GW GW GW GW GW GW GW ZAU ZAU ZAU ZAU ZAU ZAU CNRRI CNRRI CNRRI CNRRI CNRRI ZAU ZAU ZAU ZAU ZAU CNRRI CNRRI CNRRI CNRRI CNRRI CNRRI CNRRI ZAU ZAU ZAU ZAU ZAU ZAU CNRRI CNRRI CNRRI CNRRI CNRRI CNRRI 1 1 2 3 3 6 1 2 3 4 6 6 2 2 4 4 7 2 2 3 4 4 6 7 1 2 5 7 7 2 1 1 4 4 11 Chromosome RG811–R210 C131–RG472 RZ599–RZ476b RZ403b–RG482 CDO795a–RZ474 C235a–G294d RZ14–C944b RZ446b–RZ446a G249–RG418 RG143–G177 RZ667–C235a RG653–RZ508 RZ260–RZ273 G1327–RG634 Ph–G379 C949–RG449 RG678–G20 RG256–RZ260 RZ273–RG139 RG348a–C636x G379–RZ740 G271–C949 G1314b–HHU37 C586–CDO405 RZ382–RG532 RZ446a–RG654 R569a–RG13 RG29–G370b RG30–RG29 RZ386a–DO718 CDO348–CDO226a RG472–RG447 RZ590b–RG214 RG1094e–Y1065Lc RZ537b–RG16 QTLi Marker interval 6 4 9 3 6 8 9 3 11 12 10 12 2 11 6 7 7 12 3 3 7 11 8 9 2 4 10 10 11 11 6 11 8 6 12 Chromosome G1314b–HHU37 RG1094e–Y1065Lc CDO82–CDO226b RZ474–C746 C–G200a RZ143–C825 CDO82–CDO226b G249–RG418 RZ536a–L457b RG20q–RG91q G89–G1084 G1106–RG901 RZ386a–CDO718 C975–RG1022 RG653–RZ508 CDO385–C285 RG29–G370b RZ257–RZ797a RZ284–RZ403b CDO337–C944a BCD855–CDO385 RZ797b–RG1094d C424b–RZ143 R662b–G103a RZ273–RG139 G271–C949 RG752–RG1094f RG1094f–C16 G44–RG1094b RG1094b–RZ53 G200a–RZ667 RZ53–RZ781 C1073a–G187 RZ682–C236 RG901–G402 QTLj Marker interval 2.6 6.08*** ⫺1.23* 0.96*** 7.72*** 0.3 6.74 6.2 7.22 3.97 2.7 7.02 5. J.47*** R 2 (%) aaij ai and aj are the main effects of the loci i and j.5 10. .65 3.55*** 0.09 4.9 ⫺0.6 13.7 7.6 9.02 3.18*** 1.40 3.001.3 8.36*** 0.80*** 0.39*** 0.9 9.56 3.90*** ⫺0.3 8.50*** ⫺0.29* ⫺0.42*** ⫺0.08*** 1.20 4.36* ⫺0.29* ⫺0. and aaij is the epistatic effect between loci i and j.1 8.49*** 0.52*** 0.43*** 0. ** Significance levels of P ⬍ 0.52*** 0.3 9.42* ⫺0.2 5.70 4. Luo et al.27*** 1.5 5.84 4.30 3.6 ⫺1.45 3.05 7.83 3.05.2 7.84*** ⫺0.

9% in the Z413F1s. at which the Teqing allele was associated with increased GP. For GP. Twelve of the 25 epistatic effects were positive and the remaining 13 were negative. Eight of the epistatic loci (chromosomes 3. respectively.6 and 45. 48.6 and 37.2 and 30. 2001). and 18. 7 of the epistatic effects were positive and the other 4 were negative. Genetic basis of inbreeding depression and heterosis for the three yield components: In our previous article. and the remaining four appeared overdominant (all four associated with increased PP).4 and 29.2% in the LTBCF1s. h2 estimates (GY ⬍ GP ⬍ PP Ⰶ GW. and 42. five of which increased GP and the other three of which reduced GP.Inbreeding Depression and Heterosis in Rice. which indicated that more complex traits tend to be determined by a greater number of and more complex epista- . Table 7 shows 19 epistatic QTL pairs affecting GP identified from the F1 mean and/or heterosis of the BC/testcross populations. while the remaining 5 were additive as they were detected only from the F1 mean values. which explained. however. seed size is expected to contribute little to plant survival since the common grain sizes of most cultivars contain an excess of endosperm as a result of long-term artificial selection. Seventeen of the epistatic QTL pairs appeared to be overdominant. respectively. the maineffect QTL accounted for a slightly greater portion of the total variation for the yield components than for grain yield. 8. Nine of the epistatic QTL effects were positive and the remaining three were negative. This was consistent with our previous results from the F4 progeny of the Lemont/Teqing cross. we reached two conclusions regarding the genetic basis of inbreeding depression and heterosis for grain yield and biomass for the same five mapping populations (Li et al. 57. 5 in the Z413F1s. 4.8 and 18. including 8 in the LTBCF1s. Three of the epistatic QTL (on chromosomes 2. Six of the epistatic QTL effects were positive and the remaining six were negative.3% in the TQBCF1s.6% in the IR64F1s. including 9 in the LTBCF1s. respectively. seed abundance plays a much greater role for plant survival in nature than seed size. including 6 in the LTBCF1s. II on PP.8 and 46. The Teqing allele at two of the QTL resulted in increased PP while the Lemont allele caused increased PP (Table 5). Significant main effects were detected at nine of the epistatic loci (chromosomes 1. while the remaining 2 were additive. 5 in the TQBCF1s. Eleven of the epistatic QTL pairs were additive and the remaining 18 appeared to be overdominant. For the additive epistatic QTL. 5 in the Z413F1s. although the IR64F1 population showed significant heterosis for GW.6 and 49. 6. For grain crops such as rice. The first conclusion that the prevalent epistasis for the loci involved appeared to hold true for the three yield components.2 and 84.0% in the Z413F1s. and 7 in the IR64F1s. The allele at one of the QTL for increased GW was from Teqing while the other was from Lemont. Epistatic QTL associated with heterosis for the yield components in the BC and testcross populations: Table 6 shows 25 epistatic QTL pairs affecting PP identified from the F1 mean and/or heterosis of the BC/testcross populations. The overall magnitudes of hybrid breakdown and heterosis for the yield components were much less pronounced than grain yield itself (Li et al.2% of the total phenotypic variation in the RILs in the two locations. The proportions of the total phenotypic variances of the F1 mean and heterosis values explained by the epistatic QTL pairs were 51. 5 in the TQBCF1s.7 and 42. 2001). Ten of the 19 epistatic effects were positive and the remaining 9 were negative. and 7) showed significant main effects. 2.7% in the TQBCF1s. 38. 6 in the TQBCF1s. and 11) showed significant overdominance effects.1 and 64. In evolution.2% in the IR64F1s. The proportions of the total phenotypic variances of the F1 mean and heterosis values explained by the epistatic QTL pairs were 64. 5. DISCUSSION AND CONCLUSIONS The observed hybrid breakdown of the RILs and heterosis of the BC/testcross F1 populations were highly significant for PP and GP but not for GW. five of which were additive. data not shown). This tendency toward more complex fitness or yield traits showing much greater levels of heterosis and inbreeding depression has been universally observed in both plants and animals. 10 epistatic effects were positive and the remaining 8 were negative.9 and 28. 6.3% in the TQBCF1s. which explained 49. 12 pairs (5 in ZAU and 7 in CNRRI) of epistatic QTL were identified. and 7 in the IR64F1s. respectively. 41.1% in the LTBCF1s.5% of the total phenotypic variation of the RILs in ZAU and CNRRI. The observed levels of hybrid breakdown or heterosis were GY ⬎ GP ⬎ PP Ⰷ GW and so were their contributions to grain yield and the amounts of variation. 40.1% in the IR64F1s. and 3 in the IR64F1s.5 and 33. The opposite was true for their heritability.0% in the LTBCF1s. 6.7% in the Z413F1s. and 7) had significant main effects on GP. For GW. respectively.9 and 58. Five of the epistatic loci (chromosomes 1. 35. Our results indicated that the epistatic QTL explained a much greater portion of the total variation than the main-effect QTL for the yield components. 7 in the Z413F1s. 12 pairs (6 in each of the locations) of epistatic QTL were identified. and 44. Twenty of the epistatic QTL pairs appeared to be overdominant. and 12). respectively. Relatively speaking. 9. respectively. Two of the epistatic QTL (on chromosomes 1 and 6) had significant main effects on GW. Table 8 shows 29 epistatic QTL pairs affecting GW 1763 detected from the F1 mean or heterosis of the BC/ testcross populations. 40. 9.1 and 40. The proportions of the total phenotypic variances of the F1 mean and heterosis values explained by the epistatic QTL pairs were 54. For the overdominant ones. respectively.

16 3.6 5.001.11 2.64*** 0. ** Significance levels of P ⬍ 0.73 5.37 4.02*** 9.1 17.77*** 0.3 ⫺0.9 5.67 5.42* aaij 3.6 12.58*** ⫺0.57 2.39 4.34* ai 4.05.2 ⫺0.84 3.84 4.0 10.6 7.42 4.4 R 2 (%) ⫺0.62** aaij HMP ai and aj are the main effects of the loci i and j.0 7. .55 2.0 10.5 5.50 4.83*** 0.7 13.95*** 0.73 3. Chromosome Pop.3 10.66** 0. estimated by the difference between heterozygote.6 8.66*** 0.9 7.79*** 0.81*** 0.8 9.1 1 2 2 5 6 8 9 3 3 4 4 9 1 2 4 6 8 1 1 2 3 4 1 4 LT LT LT LT LT LT LT LT TQ TQ TQ TQ TQ Z413 Z413 Z413 Z413 Z413 IR64 IR64 IR64 IR64 IR64 IR64 IR64 C112–RG236 CDO118–CDO455 RZ273–RG139 RG104–C515 HHU39–RG143 RZ801–RZ14 RG449–RZ69 RZ288–C131 RG256–RZ260a HHU39–RG143 C236–RG653 C1073a–G187 RG341b–C74a CDO795a–RZ474 RG449–RZ69 RZ69–RG190 RG570a–RG451 RZ14–C944b RG140–RZ288 RG256–RZ260a RZ260a–RZ273 RG556–gl1 RZ762–C76 G56a–R662a G103b–RZ698 4 3 8 10 5 2 11 12 4 8 12 9 6 6 6 6 12 3 9 2 9 10 6 10 11 Chromosome Ph–G379 C74a–RG450 G104–G1314a G1084–RZ400 RG556–gl1 RG520–RZ446b L457b–G2132b RZ397–RZ257 G379–RZ740 C1073a–G187 RG91q–RG341a RZ777–CDO82 RG653–RZ508 RZ762–C76 G1314b–HHU37 C–G200a RG869–L102 C746–CDO337 G103b–RZ698 G45–RZ386a RZ698–G95 C16–RG561 G294a–G1468b RZ400–RG241a RZ900–G44 QTLj Marker interval 3.78 5.88*** ⫺0.38* aj 1.62** ⫺0.54 3. the homozygote in the BCF1 populations (LT and TQ).33 2.1 6.1 10.69 2.34* 0.3 12.06 4.31 5. aaij is the epistatic effect between loci i and j.01*** 0.57 2.83*** 0.78*** ⫺1.87*** ⫺0.06 R 2 (%) LOD ⫺0.8 8.1 7.95*** ⫺1.44** 0.60*** 0.71*** 0.75*** ⫺0.82 6.74*** ⫺0. J.51** aI F1 6.46 2.52** 0.1 9.2 9. as defined by Mather and Jinks (1982).68 5.4 13.07*** ⫺0. Luo et al.1 14.91*** ⫺0.09 4.44 5.81*** 0.85 3.83*** 1.4 9.78 3.83*** 0.8 7. * Significance levels of P ⬍ 0.87*** ⫺0.25 LOD 0.83*** 0.58 5.75 4. *** Significance levels of P ⬍ 0.64 ⫺0.52 4.05 3.68 3.34 3.04*** 1.88*** 0.72 4.9 ⫺0.45* 5.76*** 11.95*** 14.71 2.3 11.8 13.5 6.2 3.98 3.00*** 0.5 ⫺0.5 7.71 0.1 13.40* aj ⫺0.46** 8.4 0.44** 0.80*** ⫺0.3 10. and by the differences between the two heterozygotes (tester/Teqing ⫺ tester/Lemont) in the testcross populations (Z413 and IR64) using the F1 mean and HMP measurements.85*** ⫺0.0 10.4 10.1 7. QTLi Marker interval Digenic epistatic QTL affecting F1 hybrid performance and heterosis (HMP) of panicles/plant (PP) detected in the Lemont (LT)/Teqing (TQ) BCF1 (RILs ⫻ LT and TQ) and two testcross F1 (RILs ⫻ Z413 and IR64) populations TABLE 6 1764 L.0001.94 4.53** 0.9 6.86*** ⫺0.51** 0.

35 2.28 0.5 7.36 4.10 2.68 4.00*** 1.44*** 0.27*** ⫺0.05.64 LOD F1 5.38** ⫺0.43** ⫺0. LT LT LT LT LT LT TQ TQ TQ TQ TQ TQ TQ Z413 Z413 Z413 Z413 Z413 IR64 IR64 IR64 Pop.4 10. estimated by the difference between heterozygote. the homozygote in the BCF1 populations (LT and TQ).4 2.70*** 0. as defined by Mather and Jinks (1982).55*** 0.14 aj ⫺0.20* 0.19* 0.65 4.0 10.61 R (%) LOD 2 4.0 4.03*** aI 3. * Significance levels of P ⬍ 0.6 6.27* 1.67 3.42** 0.81 5.40** ⫺0.26** 0.16 4.45** ⫺0. and by the differences between the two heterozygotes (tester/Teqing ⫺ tester/Lemont) in the testcross populations (Z413 and IR64) using the F1 mean and HMP measurements.57 2.90 2.32** 0.19 ⫺0.68** ⫺1.1 6.54*** aaij 2.80*** 1.1 12.52*** 0.58*** ⫺0.05 2.1 1 3 5 6 9 1 1 4 4 4 3 5 1 1 1 2 4 3 4 8 C112–RG236 R210–RZ382 RG450–RG100 RG556–gl1 RZ762–C76 RZ777–CDO82 RG462–CDO118 CDO455–RZ776a HHU39a–RG143 G177–RZ590b RG214–Ph C746–CDO337 RG556–gl1 RZ14–C944b CDO118–CDO455 C131–RG472 RG139–C624x Ph–G379 G249–RG418 G177–RZ590b C825a–CSU754 11 2 8 8 8 10 6 1 11 6 11 6 11 6 5 4 8 8 11 11 11 Chromosome RZ53–RZ781 RG83–G1327 G187–G56a C424b–RZ143 G187–G56a C16–RG561 G200a–RZ667 RG472–RG447 RG16–RZ797b RG424–G1314b RZ781–C975 G1314b–HHU37 RG1109–RZ537b G1468b–RG424 Y1049–R569a RG1094e–Y1065Lc C825a–CSU754 G187–G56a RG1109–RZ537b RG16–RZ797b RZ797b–RG1094d QTLj Marker interval 2.2 10.6 5.07 4.7 4.8 4.0 17.9 9.39** 0.07*** 0.29** ⫺0.42 ⫺0.36 ⫺0.2 13.50* 3.64*** ⫺0.95 4.47** ⫺0.35** ⫺0.67*** 0.26** ⫺0.50*** 0.63*** ⫺0.0 4.73** 4. *** Significance levels of P ⬍ 0.9 8.5 5.2 16.0001. II 1765 .72** 3.27 4.5 9.99*** 0.35** ⫺0.4 8.14** ⫺1.34** ⫺0.001.11 2.3 10.42** ⫺0.31 3.47** 0.1 12.53*** aaij 2.21 3.5 3.1 13.3 6.89 ⫺0.41 0.38 2.5 R 2 (%) ai and aj are the main effects of the loci i and j.28 3.50*** 0.88 aj ⫺1.15 2.8 5.36*** ⫺0.81** 0.31*** ai HMP 4. aaij is the epistatic effect between loci i and j.9 14.46** 0.4 5.32** 0.99 0.16 2.5 6.3 8.7 7. ** Significance levels of P ⬍ 0.4 8.4 5.20* ⫺0.03 3.33*** ⫺0.27** 0. Chromosome QTLi Marker interval Digenic epistatic QTL affecting F1 hybrid performance and heterosis (HMP) of grains/plant (GP) detected in the Lemont (LT)/Teqing (TQ) BCF1 (RILs ⫻ LT and TQ) and two testcross F1 (RILs ⫻ Z413 and IR64) populations TABLE 7 Inbreeding Depression and Heterosis in Rice.27* 5.2 7.4 6.44 2.3 2.22 3.38 3.4 6.

3 16.85 2.8 1.37 4.11*** ⫺0. and by the differences between the two heterozygotes (tester/Teqing ⫺ tester/Lemont) in the testcross populations (Z413 and IR64) using the F1 mean and HMP measurements.0 6.39*** 0.55 3.66*** 2.40 8. as defined by Mather and Jinks (1982). g) detected in the Lemont (LT)/Teqing (TQ) BCF1 (RILs ⫻ LT and TQ) and two testcross F1 (RILs ⫻ Z413 and IR64) populations TABLE 8 1766 L.2 10.97*** 1.42 5.9 ⫺1.1 5.6 ⫺0.3 10.1 10. *** Significance levels of P ⬍ 0.05 3.09 5.1 6.67** 0.89** 6.50 2.51*** 0.99 7.93*** 10.1 5.81*** 6.14*** 4.9 ⫺0.30* ⫺0.4 4.73 6.02*** 0.09 5.59 0.2 7.81 2.0 7.54** 0.47 0.83** 0. ** Significance levels of P ⬍ 0.1 10.92*** ⫺1.7 5.9 12.66*** 0.58 LOD HMP ai and aj are the main effects of the loci i and j.77*** 0.37 3.57** 0.7 4. QTLi Marker interval Digenic epistatic QTL affecting F1 hybrid performance and heterosis (HMP) of 1000 grain weight (GW.46* 0.50** 0.86*** 2.1 ⫺0.6 13.61*** 0.92 2.80*** ⫺1.42 3.19*** ⫺0.44 2.72*** 3.96 0. the homozygote in the BCF1 populations (LT and TQ).64** ⫺0.60 4. Luo et al.5 ⫺0.77** 0.82 2.85*** 14. .94 3.0001.63 5.05.3 11.3 7.20 2.58** 0.7 6.63 3.64*** 0.8 R 2 (%) 2.8 9.46** 8.94 ⫺0. estimated by the difference between heterozygote. aaij is the epistatic effect between loci i and j.9 18.2 8.75** ⫺0.06 4.60*** ⫺0. J.58 6.06*** 1.51 6.41 2.20 4.0 5.91*** ⫺1.5 6.0 9.5 27.1 2 2 4 5 6 6 6 7 1 2 2 5 5 8 1 3 4 5 6 8 8 1 1 2 3 4 4 6 LT LT LT LT LT LT LT LT LT TQ TQ TQ TQ TQ TQ Z413 Z413 Z413 Z413 Z413 Z413 Z413 IR64 IR64 IR64 IR64 IR64 IR64 IR64 RG957–RG462 CDO348–CDO226a G1327–RG634 RG482–CDO795a RG1094e–Y1065Lc RG1094e–Y1065Lc G1314b–HHU37 RZ288–C131 C515–RG348a RG214–Ph RG556–gl1 G1314b–HHU37 G1314a–G2140 RZ323a–C225c RG236–RZ801 RG83–G1327 C624x–G45 RG556–gl1 R569a–RG13 C225c–G2132a C944b–RG957 RZ476a–RZ599 G45–RZ386a G177–RZ590b RG13–CDSR49 RG653–Z508 HHU37–RZ682 RZ516–RZ2 RG29–G370b 1 12 11 6 8 9 9 10 6 9 6 7 10 12 8 3 8 9 8 12 5 3 5 11 12 7 9 9 8 Chromosome RZ288–C131 RG20q–RG91q RZ900–G44 G1314b–HHU37 C225c–G2132a CDO395–CDO1081 RG570a–RG451 RG561–C223 RG424–G1314b RZ777–CDO82 G294d–G294a BCD855–CDO385 RG561–C223 G1106–RG901a C1073a–G187 C746–CDO337 G187–G56a RZ698–G95 G104–G1314a RG901a–G402 RG13–CDSR49 RG348a–C636x RG13–CDSR49 G44–RG1094b G1106–RG901a RG29–G370b G95–R662b RG451–RZ404 G187–G56a WTLj Marker interval 4. * Significance levels of P ⬍ 0.6 9.77*** 5.10 aj R 2 (%) aI aaij LOD F1 0.90 3.69*** 0.6 7.86*** 1.01*** ⫺0. Chromosome Pop.90*** ⫺1.30* ai 1.29*** aaij 4.76 2.001.2 13.5 aj ⫺0.29 3.32 3.86*** 3.59 2.4 ⫺0.

2% in the BC/testcross populations) occurred between complementary loci with no detectable main effects. epistasis occurred between a main-effect QTL and a complementary locus and in only one case between main-effect QTL. there is a major dilemma regarding how inbreeding depression is explained by the overdominance theory in which the mutation load is at the minimum (Crow 1999). while the commonly observed heterosis is often 30% or greater in maize. to the strong natural . Moreover. the QTL effects for yield and the components were in the same direction for increased trait values (and grain yield). or equal to.0% in the BC/testcross populations). we found that this was generally true for most quantitative traits studied in these populations except heading date. Our second conclusion (Li et al. 12 (44. at least in our study. Similar to the grain yield (Li et al. 1997a). while the other exhibited additive gene action and did not contribute to the trait heterosis. data not shown). which suggests that apparent overdominance at QTL for grain yield might actually result from the multiplicative actions of tightly linked yield component QTL with opposite effects on yield.4%) were associated with the main-effect QTL for one of the yield components (8 for GP. we found that. It is interesting to note that QTL affecting GW could be divided into two independent groups. our results provide an adequate explanation. In many fewer cases (17. this latter group of genes accounted for 28. Also. Thus. suggesting that the overdominant QTL for grain yield were due to the pseudooverdominance from the repulsive linkage of completely or partially dominant QTL for yield components. However. The significant genetic overlap. there was no evidence. 10 (41. 5% of the yield heterosis in maize. Thus. which is most likely due to overdominance. of the 24 overdominant epistatic QTL pairs affecting yield. This suggested that these QTL were overdominant. our results provide strong evidence for the presence of pronounced epistasis for grain yield or fitness-related traits in rice. inbreeding depression in rice contains two parts. Crow (1999) pointed out that the dominance hypothesis can explain. The first group showed primarily nonadditive gene action and explained 62. 1997a). at most.1% of the total variation in the trait heterosis (average across the four BC/testcross populations). In fact. Similar to grain yield.Inbreeding Depression and Heterosis in Rice. and 2 for GW). Stuber 1994.7%) were attributed to the overdominant QTL pairs affecting GP.4% in the RILs and 77. the parameters at most main-effect and epistatic QTL estimated from the heterosis values were greater than. the same general pattern of epistasis affecting the yield components was revealed for the yield components. which has been suggested by a large number of empirical studies in other selfing and outcrossing plant species (Allard 1988. As discussed in our previous article (Li et al.6% in the RILs and 21. This result resembles the observation in the F4 progeny of the same cross (Li et al. 2001). it is difficult to distinguish the 1767 true overdominance from pseudooverdominance generated by repulsion-phase linkage between genes of partial or complete dominance (Crow 1952. which was consistent with the relatively high heritability of GW observed in this study and many previous studies. Tables 4–8). and 9). the overdominant main-effect QTL affecting two of the components were mapped to the same locations of the yield QTL in the same population. 2001). 1997). the nonadditive genetic component resulting from disappearance of overdominance due to homozygosity and the additive genetic one arising from breakdown of co-adapted indica or japonica gene complexes by recombination and homozygosity. It would be even less likely that the apparent overdominance at large numbers of the observed epistatic QTL was all attributable to pseudooverdominance. On average. When we looked closely at the correspondences of the main-effect QTL affecting grain yield and its components (Figure 2. In only three cases (chromosomes 4. 2001) that overdominance is an important property of most loci associated with heterosis for grain yield also appeared to hold true for the three yield components. in magnitude. of the 22 overdominant main-effect QTL affecting grain yield. as indicated by Goodnight (1999).e.1% of the total trait variation of the F1 mean values (Tables 6–8). The apparent overdominance at both main-effect and epistatic QTL for grain yield and its components observed in the four related BC and testcross populations was overwhelming. for which more main-effect QTL showing partial or complete dominance were detected (Li 2001. Similarly. 6. 2 for PP. Because of the resolution of 10–20 cM of our molecular linkage map. but the QTL effects were in the same direction for increased trait values in all three cases. the epistatic effects were in the same direction for yield and GP. i. many empirical studies indicate the presence of negative correlation between grain yield components. The predominance of epistasis between complementary loci observed in this study suggests that fitness traits and grain yield are associated more with multilocus genotypes than with specific alleles at individual loci. and in all cases. In all cases.. In this respect. Accurate detection and parameter estimation of epistasis then can be more easily achieved by direct comparison of differences among multilocus genotypes using reduced genetic models (Li 1997). revealed by correlation analyses. it is expressed more often as a common feature of multilocus genotypes than as the allelic interaction at single main-effect QTL (Crow 1952). those from the F1 mean values for GP and PP. Lamkey and Edwards 1999). most epistasis (79. II sis (Li et al. by selfing. One may imagine that the genetic load from recessive mutants of large deleterious effects in genomes of selfing plant species such as rice should be at the minimum because of its quick exposure. between genes for heterosis and hybrid breakdown indicates that epistasis is the key for resolving this dilemma.

associated with hybrid breakdown of the Lemont/Teqing recombinant inbred lines and heterosis of their two BCF1 and two testcross F1 populations. Luo et al. Symbols divided by horizontal lines are epistatic QTL having significant main effects on the yield components. 1768 L. J.—Genomic locations for main-effect QTL affecting grain yield and its components.Figure 2. .

II .1769 Figure 2. Inbreeding Depression and Heterosis in Rice.—Continued.

Bruce. 213– 223 in Principles of Plant Breeding. Tansley and S. we found that none of the top 20 highyielding RILs had high levels of trait heterosis and very few of them resulted in top high-yielding BC/testcross F1 hybrids. with emphasis on increased panicle size (more grains per panicle). Crow.. B. pp. 1910 The Mendelian theory of heredity and the augmentation of vigor. prediction of yield heterosis of hybrids using either molecular markers or phenotypic values of parental lines would be impossible because of the complexity of the genetic basis associated with heterosis. 119–130 in Molecular Analysis of Complex Traits. ASA-CSSA-SSSA Societies. Coors and S. D. Mei were also supported by the RF fellowships. there is no sign for a corresponding decrease in heterosis for most maize hybrids (Duvick 1999). 2001). G. Luo. WI. should be much more efficient than selecting for single components. edited by J. pp. pp. Pandey. simultaneous selection for all three yield components. were much greater for panicle size than for panicle number and grain weight. Coors and S. Z.. 59–68 in The Genetics and Exploitation of Heterosis in Crops. Pandey. Ames. IA. 282–297 in Heterosis. L. F. numerous classic genetic studies have clearly shown that the phenotypic relationships between yield and its components in grain crops are complex and that the genetic basis of the relationships in segregating breeding populations remains poorly understood. It should be pointed out that as the collective effect on a specific trait. Even with such an increase in the yield level of maize inbreds. W. J. 49–58 in The Genetics and Exploitation of Heterosis in Crops. 69–80 in The Genetics and Exploitation of Heterosis in Crops. which is based on the expected contributions of component traits to yield. Gowen. L. W. D. J. one would have to explain why selection should favor such a high level of genetic load across the rice genome maintained by repulsion linkage (Li et al. J. edited by J.” suggesting that separate efforts should be taken for breeding high-yielding inbred and hybrid cultivars in rice. of all genes showing nonadditive action. and artificial selection for increased yield (and fitness). edited by A. Science 32: 627–628. heterosis very often stands for complex fitness-related traits of economic importance. Thus. pp. and the contribution to grain yield. 79: 225–238. N. Madison. However. WI. unless the other alternative hypotheses are adequately tested (Xiao et al. 19–29 in The Genetics and Exploitation of Heterosis in Crops. edited by J.. Allard. elevated recombination in breeding populations by outcrossing. J... pp. edited by J. Li and A.. M. In this study. 1960 Inbreeding depression and heterosis. results of complete or partial dominance at maineffect QTL for yield components and other quantitative traits may not provide sufficient evidence supporting the dominance theory of heterosis. Second. C.. 1936 Heterosis. K. This is so because the levels of heterosis and genetic variation in the segregating populations (particularly for intersubspecific crosses). Boca Raton. Ed. LITERATURE CITED Allard. pp. FL. H. edited by J. Luo et al. London/New York. L. and H. while genes/QTL affecting the three yield components appeared to be independent. ASA-CSSA-SSSA Societies. This is because strong and long-term selection for increased yield. WI. Z. ASA-CSSA-SSSA Societies. Paterson. CSSA Special Publication no. Duvick. WI. although epistasis has not been adequately tested and characterized in most of these species. even though to most plant and animal breeders. K. pp.. 73) that “Strong inbreeding depression will result in a high heterosis expression. Filho. G. heterosis is part of the genetic basis of that trait. J. W. G. S. East. Lamkey.. 1999 Epistasis and heterosis. Madison. Also.1770 L. 1999 Quantitative genetics of heterosis. G. First. K.. Hered. Iowa State College Press. it would be expected that the genetic basis of heterosis may vary considerably. Pandey. 1–12 in Concepts and Breeding of Heterosis in Crop Plants.. K.. Goldman. B. Wang. Madison. Implications for rice improvement: Indirect selection for grain yield components to improve yield potential in grain crops has been a common selection strategy practiced by many plant breeders. 1997 Molecular analysis of epistasis affecting complex traits. it is not unlikely that the pronounced epistasis and overdominance we observed in rice may have played an important role in the heterosis observed in maize and other plant and animal species. S. edited by J. depending on specific traits and materials involved. and reinforced selfing for development of inbred parents should have eliminated most deleterious mutants. S. E. Madison. Genetics 21: 375–397. Finally. This argument is evidenced by the many-fold increase in the yields of the current maize inbreds since the beginning of the century (Duvick 1999). This result is consistent with empirical experiences with the common rice hybrid cultivars (Zeng et al. M. Coors and S. Edwards. J. and J. ASA-CSSA-SSSA Societies. J. Coors and S. Madison. Paterson and by a grant from the Chinese Ministry of Agriculture to C. WI. 1981 Introduction to Quantitative Genetics. F. pp. Crow. John Wiley & Sons. A. Falconer. 1998 From out of old fields comes all this new corn: an historical perspective on heterosis in plant improvement. Li. D. W. 25. New York. pp. McCouch of Cornell University and the Japanese Rice Genome Research Program for providing us with DNA probes. 1999 Dominance and overdominance. 1988 Genetic changes associated with the evolution of adaptedness in cultivated plants and their wild progenitors. G. . the genetic load from recessive deleterious mutants in the current maize populations is expected to be low. ASA-CSSA-SSSA Societies. Results from this study have several implications for rice breeding for improved yield potential. selection for improved yield potential of parental lines may not necessarily result in the expected gain in the hybrids. 31–48 in The Genetics and Exploitation of Heterosis in Crops. 2. R. 1979). CRC Press. Longman. This coincides well with Filho’s statement (1999. 1999 Inbreeding depression and heterosis. 1999 Heterosis: feeding people and protecting natural resources. Li. 1952 Dominance and overdominance. J. We are grateful to Drs. p. Ying and L. R. Pandey. Pandey. Coors and S. W.. Otherwise.. This research was supported by a grant from the Rockefeller Foundation to Z. H. I. 2001 QTL mapping in rice: a few critical considerations. R. According to evidence from numerous classical quantitative genetic studies. Thus. 1994). Goodnight. Luo. to break the yield ceiling of hybrid rice cultivars.

I. W. N. K. 1771 Shull. and J. W. WI. Boca Raton. M.. Genetics 158: 1737–1753. H. Xu. Z. Park and J. Zeng . L. T. Ed.. Genet. Coors and S.. P. Whitehead Technical Report. D. Stuber. Yang. X. Acad. Pinson. 1908 The composition of a field of maize. Li. 1997 Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Mather. H. Li. The Philippines (in press). Pinson. 1982 Biometrical Genetics. D. W. 261: 58–63. SAS Institute. J. W. 4: 296–301. Chapman & Hall. Genetics 145: 453–465. Luo. R. J. Q. NC. Stansel. W. 1999 Mapping QTLs with epistatic effects and QTL ⫻ environment interactions by mixed model approaches. M. H. S. Proceedings of the 4th International Rice Genetics Symposium. Pandey. Gen. C. Xiao. Yuan and S. K. USA 94: 9226–9231. H. Stuber. Lander. 2001 Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. S. Stansel and W. W. Daly and E. Genetics 132: 832–838. L. SAS Institute. G. Theor. K.. Appl. 1992 Constructing genetic maps with MAPMAKER/EXP 3. Williams and R. Wang. 1997 Case history in crop improvement: yield heterosis in maize. H. 99: 1255–1264. CRC Press. J. Z. 1997b Genetics of hybrid sterility and hybrid breakdown in an inter-subspecific rice (Oryza sativa L. L. Los Banos. P. Moll. Zhu. H. W.. R.. Stuber. Genetics 140: 745–754. Lincoln. J. Plant Breed. Tan. Acta Crop Scientia Sinica 5(3): 23–34. London/New York.. 1999 A ‘defeated’ resistance gene acts as a QTL against a virulent strain of Xanthonomas oryzae pv.. G. D. L.. C. edited by A. F.. Ann. C. Breed. K. Stansel. H. H. D. Communicating editor: Z-B. 1997a Epistasis for three grain yield components in rice (Oryza sativa L.S. Paterson. Mei. Li. Park and J. Crop Sci. Significance in predictions of hybrid performances. D.0. H. 1999 Research need in heterosis. Z. M. A. edited by J. C.. FL. Z.. Theor. W. pp. Park. Li. K. Longman Group. G. Stuber. Gao et al.. R. Mol. Y. Mei. Y. D. Lincoln. 3. S. Tanksley. 1973 Epistasis in maize (Zea mays L.. Shu. R. et al. L. H. Genet. Z. W. Appl. J. S. C. Tabien. 1994 Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. W. Li. Rev. Wolff.. J. L. Ed. 1996 SAS Users Guide: Statistic. 1979 Principles of Crop Improvement.). Zeng. Sci.) population. Paterson. IRRI. 1994 Heterosis in plant breeding.. Luo. X.. Wang. Cary. Y. Z. 91: 374–381. W. S..): III. S. L. II Rice Genetics VI. W. J. Q. London and New York. Proc. Lu and X. W. Yu. 3. E. 1979 Relationships between F1 heterosis and their parental performance in rice. Assn. Genetics 145: 1139–1148. Li. Genet. pp.. Pinson. W. D.-K. Li and A. R. Natl. M. 12: 227–251. Paterson et al. 13: 195–200. Helentjaris and E. Simmonds. 1992 Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Madison. Phillips. B. Jinks. Li.. A. ASA-CSSA-SSSA Societies.Inbreeding Depression and Heterosis in Rice. Lander. Biomass and grain yield. K. 501–508 in The Genetics and Exploitation of Heterosis in Crops. Paterson. A. S. 197–205 in Molecular Dissection of Complex Traits. Z. oryzae. Paterson. 1995 Identification of QTL for heading date and plant height in rice using RFLP markers.. J.