Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid (hybrid vigorymolecular markersyquantitative trait lociyinteraction between loci)

The genetic basis of heterosis was investi- gated in an elite rice hybrid by using a molecular linkage map with 150 segregating loci covering the entire rice genome. Data for yield and three traits that were components of yield were collected over 2 years from replicated field trials of 250 F2:3 families. Genotypic variations explained from about 50% to more than 80% of the total variation. Interactions between genotypes and years were small compared with the main effects. A total of 32 quantitative trait loci (QTLs) were detected for the four traits; 12 were observed in both years and the remaining 20 were detected in only one year. Overdomi- nance was observed for most of the QTLs for yield and also for a few QTLs for the component traits. Correlations between marker heterozygosity and trait expression were low, indicat- ing that the overall heterozygosity made little contribution to heterosis. Digenic interactions, including additive by additive, additive by dominance, and dominance by dominance, were frequent and widespread in this population. The interactions involved large numbers of marker loci, most of which indi- vidually were not detectable on single-locus basis; many interactions among loci were detected in both years. The results provide strong evidence that epistasis plays a major role as the genetic basis of heterosis. The two earliest hypotheses regarding heterosis, both pro- posed in 1908—i.e., the dominance hypothesis (1) and the overdominance hypothesis (2, 3)—have competed for most of this century (4). However, pertinent data allowing for critical assessments of these hypotheses remained largely unavailable until very recently with the advent of discretely recognizable mendelian markers such as allozymes, restriction fragment length polymorphisms (RFLPs), and more recently high- density molecular linkage maps. Stuber et al. (5), who analyzed the genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines, observed that heterozygotes of almost all the quantitative trait loci (QTLs) for yield had higher phenotypic values than the respective homozygotes. They suggested that both overdominance and QTLs detected by single-locus analysis play a significant role in heterosis. On the other hand, Xiao et al. (6), who conducted an inheritance study of quantitative traits in an intersubspecific cross of rice, suggested that dominance may be the genetic basis of heterosis in rice. Both of the dominance and overdominance hypotheses are based only on single-locus theory. Wright (7) visualized a ''net-like'' structure of population genotypes such that the variations of most characters are affected by many loci and that each gene replacement may have effects on many characters. Based on this perspective, epistasis should be one of the most important genetic com- ponents in the inheritance of quantitative characters. Using morphological markers marking small chromosome segments, Fasoulas and Allard (8) showed that epistasis was responsible for a major part of the total genetic variance for seven of the eight characters studied in crosses between near isogenic lines of cultivated barley. Population genetic analyses have also established that epistasis, functioning to assemble and main- tain favorable multilocus genotypes, is a major mechanism of adaptation in various plant species (9). Surprisingly, however, little evidence for epistasis has been indicated in the recent data from molecular marker-based studies of yield and yield- associated characters, although epistasis has been observed in characters such as plant height in soybean, nitrogen-fixing ability in rice, and seed size in legumes (10-13). Thus, the significance of epistasis in the expression of heterosis in relation to hybrid performance has yet to be established. Rice is the staple food for a large segment of the world population. The success of hybrid rice breeding, together with saturated molecular linkage maps (14, 15) and relatively small genome size of this species, has provided a rare opportunity for dissecting the genetic basis of heterosis in elite rice hybrids. In the study reported in this paper, we investigated, at both single-locus and two-locus levels, the genetic components conditioning the inheritance of yield and yield component traits in one of the most heterotic crosses. The main objective was to characterize the genetic basis of heterosis in this hybrid with the long-term goal of manipulating the genome for hybrid rice improvement.