Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield

To understand the genetic basis of inbreeding depression and heterosis in rice, main-effect and epistatic QTL associated with inbreeding depression and heterosis for grain yield and biomass in five related rice mapping populations were investigated using a complete RFLP linkage map of 182 markers, replicated phenotyping experiments, and the mixed model approach. The mapping populations included 254 F(10) recombinant inbred lines derived from a cross between Lemont (japonica) and Teqing (indica) and two BC and two testcross hybrid populations derived from crosses between the RILs and their parents plus two testers (Zhong 413 and IR64). For both BY and GY, there was significant inbreeding depression detected in the RI population and a high level of heterosis in each of the BC and testcross hybrid populations. The mean performance of the BC or testcross hybrids was largely determined by their heterosis measurements. The hybrid breakdown (part of inbreeding depression) values of individual RILs were negatively associated with the heterosis measurements of their BC or testcross hybrids, indicating the partial genetic overlap of genes causing hybrid breakdown and heterosis in rice. A large number of epistatic QTL pairs and a few main-effect QTL were identified, which were responsible for >65% of the phenotypic variation of BY and GY in each of the populations with the former explaining a much greater portion of the variation. Two conclusions concerning the loci associated with inbreeding depression and heterosis in rice were reached from our results. First, most QTL associated with inbreeding depression and heterosis in rice appeared to be involved in epistasis. Second, most ( approximately 90%) QTL contributing to heterosis appeared to be overdominant. These observations tend to implicate epistasis and overdominance, rather than dominance, as the major genetic basis of heterosis in rice. The implications of our results in rice evolution and improvement are discussed.     

Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines

The exploitation of heterosis is one of the most outstanding advancements in plant breeding, although its genetic basis is not well understood yet. This research was conducted on the materials arising from the maize single cross B73 x H99 to study heterosis by procedures of classical genetic and quantitative trait loci (QTL) analyses. Materials were the basic generations, the derived 142 recombinant inbred lines (RILs), and the three testcross populations obtained by crossing the 142 RILs to each parent and their F(1). For seedling weight (SW), number of kernels per plant (NK), and grain yield (GY), heterosis was >100% and the average degree of dominance was >1. Epistasis was significant for SW and NK but not for GY. Several QTL were identified and in most cases they were in the additive-dominance range for traits with low heterosis and mostly in the dominance-overdominance range for plant height (PH), SW, NK, and GY. Only a few QTL with digenic epistasis were identified. The importance of dominance effects was confirmed by highly significant correlations between heterozygosity level and phenotypic performance, especially for GY. Some chromosome regions presented overlaps of overdominant QTL for SW, PH, NK, and GY, suggesting pleiotropic effects on overall plant vigor.     

Gene actions of QTLs affecting several agronomic traits resolved in a recombinant inbred rice population and two testcross populations

To understand the types of gene action controlling seven quantitative traits in rice, QTL mapping was performed to dissect the main effect (M-QTLs) and digenic epistatic (E-QTLs) QTLs responsible for the trait performance of 254 recombinant inbred lines (RILs) of "Lemont/Teqing", and two testcross (TC) F(1) populations derived from these RILs. The correlation analyses reveal a general pattern, i.e. trait heritability in the RILs was negatively correlated to trait heterosis in the TC hybrids. A large number of M-QTLs and E-QTLs affecting seven traits, including heading date (HD), plant height (PH), flag leaf length (FLL), flag leaf width (FLW), panicle length (PL), spikelet number per panicle (SN) and spikelet fertility (SF), were identified and could be classified into two predominant groups, additive QTLs detected primarily in the RILs, and overdominant QTLs identified exclusively in the TC populations. There is little overlap between QTLs identified in the RILs and in the TC populations. This result implied that additive gene action is largely independent from non-additive gene action in the genetic control of quantitative traits of rice. The detected E-QTLs collectively explained a much greater portion of the total phenotypic variation than the M-QTLs, supporting prior findings that epistasis has played an important role in the genetic control of quantitative traits in rice. The implications of these results to the development of inbred and hybrid cultivars were discussed.     

Heterotic trait locus (HTL) mapping identifies intra-locus interactions that underlie reproductive hybrid vigor in Sorghum bicolor

Identifying intra-locus interactions underlying heterotic variation among whole-genome hybrids is a key to understanding mechanisms of heterosis and exploiting it for crop and livestock improvement. In this study, we present the development and first use of the heterotic trait locus (HTL) mapping approach to associate specific intra-locus interactions with an overdominant heterotic mode of inheritance in a diallel population using Sorghum bicolor as the model. This method combines the advantages of ample genetic diversity and the possibility of studying non-additive inheritance. Furthermore, this design enables dissecting the latter to identify specific intra-locus interactions. We identified three HTLs (3.5% of loci tested) with synergistic intra-locus effects on overdominant grain yield heterosis in 2 years of field trials. These loci account for 19.0% of the heterotic variation, including a significant interaction found between two of them. Moreover, analysis of one of these loci (hDPW4.1) in a consecutive F2 population confirmed a significant 21% increase in grain yield of heterozygous vs. homozygous plants in this locus. Notably, two of the three HTLs for grain yield are in synteny with previously reported overdominant quantitative trait loci for grain yield in maize. A mechanism for the reproductive heterosis found in this study is suggested, in which grain yield increase is achieved by releasing the compensatory tradeoffs between biomass and reproductive output, and between seed number and weight. These results highlight the power of analyzing a diverse set of inbreds and their hybrids for unraveling hitherto unknown allelic interactions mediating heterosis.     

Additive and over-dominant effects resulting from epistatic loci are the primary genetic basis of heterosis in rice

A set of 148 F9 recombinant inbred lines (RILs) was developed from the cross of an indica cultivar 93-11 and japonica cultivar DTT13,showing strong F1 heterosis.Subsequently,two backcross F1 (BCF1) populations were constructed by backcrossing these 148 RILs to two parents,93-11 and DT713.These three related populations (281BCF1 lines,148 RILs) were phenotyped for six yield-related traits in two locations.Significant inbreeding depression was detected in the population of RILS and a high level of heterosis was observed in the two BCF1 populations.A total of 42 main-effect quantitative trait loci (M-QTLs) and 109 epistatic effect QTL pairs (E-QTLs) were detected in the three related populations using the mixed model approach.By comparing the genetic effects of these QTLs detected in the RILs,BCF1 performance and mid-parental heterosis (HMp),we found that,in both BCF1 populations,the QTLs detected could be classified into two predominant types:additive and over-domlnant loci,which indicated that the additive and over-dominant effect were more important than complete or partially dominance for M-QTLs and E-QTLs.Further,we found that the E-QTLs detected collectively explained a larger portion of the total phenotypic variation than the M-QTLs in both RILs and BCF1 populations.All of these results suggest that additive and over-dominance resulting from epistatic loci might be the primary genetic basis of heterosis in rice.     

Quantitative trait loci mapping for yield and its components by using two immortalized populations of a heterotic hybrid in Gossypium hirsutum L.

Quantitative trait loci (QTL) mapping provides a powerful tool for unraveling the genetic basis of yield and yield components as well as heterosis in upland cotton. In this research, a molecular linkage map of Xiangzamian 2 (Gossypium hirsutum L.)-derived recombinant inbred lines (RILs) was reconstructed based on increased expressed sequence tag–simple sequence repeat markers. Both the RILs and immortalized F2s (IF2) developed through intermating between RILs were grown under multiple environments. Yield and yield components including seed-cotton yield, lint yield, bolls/plant, boll weight, lint percentage, seed index, lint index and fruit branch number were measured and their QTL were repeatedly identified across environments by the composite interval mapping (CIM) method. From a total of 111 non-redundant QTL, 23 were detected in both two populations. In the meantime, multi-marker joint analyses showed that 16 of these QTL had significant environmental interaction. QTL for correlated traits tended to be collocated and most of the QTL for seed-cotton yield and lint yield were associated with QTL for at least one yield component, consistent with the results observed in correlation analyses. For many QTL with significant additive effects, positive alleles from CRI12, the inferior parent with lower yield performance, were associated with trait improvement. Trait performance of IF2s and the large number of QTL with positive dominant effects implied that dominance plays an important role in the genetic basis of heterosis in Xiangzamian 2 and that non-additive inheritance is also an important genetic mode for lint percentage in the population. These QTL can provide the bases for marker-assisted breeding programs of upland cotton.     

Importance of over-dominance as the genetic basis of heterosis in rice

In populations derived from commercial hybrid rice combination Shanyou 10, F₁ heterosis and F₂ inbreeding depression were observed on grain yield (GYD) and number of panicles (NP). Using marker loci evenly distributed on the linkage map as fixing factors, the F₂ population was divided into sub-populations. In a large number of sub-populations, significant correlations were observed between heterozygosity and GYD, and between heterozygosity and NP. This was especially true in type III sub-populations in which the genotype of a fixing factor was heterozygotes. In type III sub-populations, 15 QTL for GYD and 13 QTL for NP were detected, of which the majority exhibited over-dominance effects for increasing the trait values. This study showed that over-dominance played an important role in the genetic control of heterosis in rice.     

Gene actions of QTLs affecting several agronomic traits resolved in a recombinant inbred rice population and two backcross populations

To understand the types of gene action controlling seven quantitative traits in rice, we carried out quantitative trait locus (QTL) mapping in order to distinguish between the main-effect QTLs (M-QTLs) and digenic epistatic QTLs (E-QTLs) responsible for the trait performance of 254 recombinant inbred lines (RILs) from rice varieties Lemont/Teqing and two backcross hybrid (BCF₁) populations derived from these RILs. We identified 44 M-QTL and 95 E-QTL pairs in the RI and BCF₁ populations as having significant effects on the mean values and mid-parental heterosis of heading date, plant height, flag leaf length, flag leaf width, panicle length, spikelet number and spikelet fertility. The E-QTLs detected collectively explained a larger portion of the total phenotypic variation than the M-QTLs in both the RI and BCF₁ populations. In both BCF₁ populations, over-dominant (or under-dominant) loci were more important than additive and complete or partially dominant loci for M-QTLs and E-QTL pairs, thereby supporting prior findings that overdominance resulting from epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice.     

Importance of over-dominance as the genetic basis of heterosis in rice

In populations derived from commercial hybrid rice combination Shanyou 10, F1 hetero-sis and F2 inbreeding depression were observed on grain yield (GYD) and number of panicles (NP). Using marker loci evenly distributed on the linkage map as fixing factors, the F2 population was divided into sub-populations. In a large number of sub-populations, significant correlations were observed between heterozygosity and GYD, and between heterozygosity and NP. This was especially true in type III sub-populations in which the genotype of a fixing factor was heterozy-gotes. In type III sub-populations, 15 QTL for GYD and 13 QTL for NP were detected, of which the majority exhibited over-dominance effects for increasing the trait values. This study showed that over-dominance played an important role in the genetic control of heterosis in rice.     

Genetic basis of heterosis for growth-related traits in Arabidopsis investigated by testcross progenies of near-isogenic lines reveals a significant role of epistasis

Epistasis seems to play a significant role in the manifestation of heterosis. However, the power of detecting epistatic interactions among quantitative trait loci (QTL) in segregating populations is low. We studied heterosis in Arabidopsis thaliana hybrid C24 x Col-0 by testing near-isogenic lines (NILs) and their triple testcross (TTC) progenies. Our objectives were to (i) provide the theoretical basis for estimating different types of genetic effects with this experimental design, (ii) determine the extent of heterosis for seven growth-related traits, (iii) map the underlying QTL, and (iv) determine their gene action. Two substitution libraries, each consisting of 28 NILs and covering approximately 61 and 39% of the Arabidopsis genome, were assayed by 110 single-nucleotide polymorphism (SNP) markers. With our novel generation means approach 38 QTL were detected, many of which confirmed heterotic QTL detected previously in the same cross with TTC progenies of recombinant inbred lines. Furthermore, many of the QTL were common for different traits and in common with the 58 QTL detected by a method that compares triplets consisting of a NIL, its recurrent parent, and their F(1) cross. While the latter approach revealed mostly (75%) overdominant QTL, the former approach allowed separation of dominance and epistasis by analyzing all materials simultaneously and yielded substantial positive additive x additive effects besides directional dominance. Positive epistatic effects reduced heterosis for growth-related traits in our materials.