Population-based resequencing analysis of improved wheat germplasm at wheat leaf rust resistance locus Lr21

Little is known about the genetic control of heterosis in the complex polyploid crop species oilseed rape (Brassica napus L.). In this study, two large doubled-haploid (DH) mapping populations and two corresponding sets of backcrossed test hybrids (THs) were analysed in controlled greenhouse experiments and extensive field trials for seedling biomass and yield performance traits, respectively. Genetic maps from the two populations, aligned with the help of common simple sequence repeat markers, were used to localise and compare quantitative trait loci (QTL) related to the expression of heterosis for seedling developmental traits, plant height at flowering, thousand seed mass, seeds per silique, siliques per unit area and seed yield. QTL were mapped using data from the respective DH populations, their corresponding TH populations and from mid-parent heterosis (MPH) data, allowing additive and dominance effects along with digenic epistatic interactions to be estimated. A number of genome regions containing numerous heterosis-related QTL involved in different traits and at different developmental stages were identified at corresponding map positions in the two populations. The co-localisation of per se QTL from the DH population datasets with heterosis-related QTL from the MPH data could indicate regulatory loci that may also contribute to fixed heterosis in the highly duplicated B. napus genome. Given the key role of epistatic interactions in the expression of heterosis in oilseed rape, these QTL hotspots might harbour genes involved in regulation of heterosis (including fixed heterosis) for different traits throughout the plant life cycle, including a significant overall influence on heterosis for seed yield.     

DIFFERENTIAL DOMINANCE OF PLEIOTROPIC LOCI FOR MOUSE SKELETAL TRAITS

The term "differential dominance" describes the situation in which the dominance effects at a pleiotropic locus vary between traits. Directional selection on the phenotype can lead to balancing selection on differentially dominant pleiotropic loci. Even without any individual overdominant traits, some linear combination of traits will display overdominance at a locus displaying differential dominance. Multivariate overdominance may be responsible, in part, for high levels of heterozygosity found in natural populations. We examine differential dominance of 70 mouse skeletal traits at 92 quantitative trait loci (QTL). Our results indicate moderate to strong additive and dominance effects at pleiotropic loci, low levels of individual-trait overdominance, and universal multivariate overdominance. Multivariate overdominance affects a range of 6% to 81% of morphospace, with a mean of 32%. Multivariate overdominance tends to affect a larger percentage of morphospace at pleiotropic loci with antagonistic effects on multiple traits (42%). We conclude that multivariate overdominance is common and should be considered in models and in empirical studies of the role of genetic variation in evolvability.     

Gene actions at loci underlying several quantitative traits in two elite rice hybrids

To understand the gene activities controlling nine important agronomic quantitative traits in rice, we applied a North Carolina design 3 (NC III design) analysis to recombinant inbred lines (RILs) in highly heterotic inter- (IJ) and intra-subspecific (II) hybrids by performing the following tasks: (1) investigating the relative contribution of additive, dominant, and epistatic effects for performance traits by generation means analysis and variance component estimates; (2) detecting the number, genomic positions, and genetic effects of QTL for phenotypic traits; and (3) characterizing their mode of gene action. Under an F∞-metric, generation means analysis and variance components estimates revealed that epistatic effects prevailed for the majority of traits in the two hybrids. QTL analysis identified 48 and 66 main-effect QTL (M-QTL) for nine traits in IJ and II hybrids, respectively. In IJ hybrids, 20 QTL (41.7%) showed an additive effect of gene actions, 20 (41.7%) showed partial-to-complete dominance, and 8 (16.7%) showed overdominance. In II hybrids, 34 QTL (51.5%) exhibited additive effects, 14 (21.2%) partial-to-complete dominance, and 18 (27.3%) overdominance. There were 153 digenic interactions (E-QTL) in the IJ hybrid and 252 in the II hybrid. These results suggest that additive effects, dominance, overdominance, and particularly epistasis attribute to the genetic basis of the expression of traits in the two hybrids. Additionally, we determined that the genetic causes of phenotypic traits and their heterosis are different. In the plants we studied, the phenotypic traits investigated and their heterosis were conditioned by different M-QTL and E-QTL, respectively, and were mainly due to non-allelic interactions (epistasis).     

Heterosis for biomass yield and related traits in five hybrids of Arabidopsis thaliana L. Heynh

Heterosis is of utmost economic importance in plant breeding. However, its underlying molecular causes are still unknown. Given the numerous advantages of Arabidopsis thaliana as a model species in plant genetics and genomics, we assessed the extent of heterosis in this species using five hybrids derived from five ecotypes. Parents, F(1) and F(2), generations in both reciprocal forms were grown in a greenhouse experiment with four replications. Mid-parent heterosis (MPH) and best-parent heterosis (BPH) averaged across hybrids were surprisingly high for biomass yield (MPH: 60.3%; BPH: 32.9%) and rosette diameter (MPH: 49.4%; BPH: 34.8%), but smaller for flowering date (MPH: 27.5%; BPH: 18.5%), seed yield (MPH: 18.9%; BPH: 1.7%), and yield components. Individual hybrids varied considerably in their MPH and BPH values for all traits, one cross displaying 140.1% MPH for biomass yield. MPH was not associated with parental genetic distance determined from molecular markers. Reciprocal effects were significant only in a few cases. With a proper choice of hybrids, our results encourage the use of Arabidopsis as a model species for investigating the molecular causes of heterosis.     

QTL and epistatic analyses of heterosis for seed yield and three yield component traits using molecular markers in rapeseed (Brassica napus L.)

Aiming to explore the basis of heterosis in rapeseed, QTLs for yield and three yield component traits were mapped and the digenic interactions were detected in an F₂ population derived from a cross between two elite rapeseed lines, SI-1300 and Eagle, in this study. Twenty-eight QTLs were detected for the four yield traits, with only two of them detected simultaneously in the Wuhan and Jingmen environments. Additive, partial dominance, dominance, and overdominance effects were all identified for the investigated traits. Dominance (including partial dominance) was shown by 55% of the QTLs, which suggests that dominance is a major genetic basis of heterosis in rapeseed. At the P ?? 0.01 level with 1000 random permutations, 108 and 104 significant digenic interactions were detected in Wuhan and Jingmen, respectively, for the four yield-related traits using all possible locus pairs of molecular markers. Digenic interactions, including additive by additive, additive by dominance, and dominance by dominance, were frequent and widespread in this population. In most cases (78.3%), the interactions occurred among marker loci for which significant effects were not detected by single-locus analysis. Some QTLs (57.1%) detected by single-locus analysis were involved in epistatic interactions. It was concluded that epistasis, along with dominance (including partial dominance), is responsible for the expression of heterosis in rapeseed.     

Comparison of the behavioral teratogenic potential of phenytoin, mephenytoin, ethotoin, and hydantoin in rats.

Pregnant Sprague-Dawley CD rats were orally administered either phenytoin (PHT, 200 mg/kg), mephenytoin (MPH, 100 mg/kg), ethotoin (ETH, 600 mg/kg), hydantoin (HYD, 1,200 mg/kg) or vehicle (propylene glycol) on days 7-18 of gestation. Mean (+/- S.E.) maternal serum concentrations of PHT, MPH, and ETH 1 hour after dosing on gestational day 18 were 16.0 +/- 3.3, 10.7 +/- 3.0, and 65.2 +/- 10.45, respectively, and free fractions were 16%, 18%, and 11% respectively. The free fraction for PHT is similar, but was lower for both MPH and ETH than that seen in humans. Preweaning mortality for PHT, MPH, ETH, HYD, and controls was 25%, 6.3%, 12.5%, 2.0% and 0.8%, respectively. The MPH and ETH-exposed animals weighed approximately 6.6% less than controls throughout the study; the other groups did not differ significantly. PHT offspring showed increased early locomotor activity. Only PHT-exposed animals (27%) exhibited abnormal circling behavior after weaning. PHT-circlers accounted for higher levels of activity in an open-field test and for longer straight channel swimming times. PHT-circlers and noncirclers differed from one another and controls on performance of a complex (Cincinnati) maze and on the development of the air-righting reflex. Offspring prenatally exposed to MPH showed an early delay in air-righting. ETH and HYD offspring were not consistently different from controls in behavior. The data suggest the following ordinal relationship among the drugs for behavioral teratogenesis: PHT much greater than MPH greater than ETH congruent to HYD congruent to CON. The effects of PHT are consistent with previous findings. Data on the other drugs suggest that other hydantoins do not possess the behavioral teratogenic efficacy of PHT and that PHT may be unique in its effects on CNS development.     

The regulatory network mediated by circadian clock genes is related to heterosis in rice

Exploitation of heterosis in rice(Oryza sativa L.) has contributed greatly to global food security.In this study,we generated three sets of reciprocal F1 hybrids of indica and japonica subspecies to evaluate the relationship between yield heterosis and the circadian clock.There were no differences in trait performance or heterosis between the reciprocal hybrids,indicating no maternal effects on heterosis.The indica-indica and indica-japonica reciprocal F1 hybrids exhibited pronounced heterosis for chlorophyll and starch content in leaves and for grain yield/biomass.In contrast,the japonica-japonica F1 hybrids showed low heterosis.The three circadian clock genes investigated expressed in an above-high-parent pattern(AHP)at seedling stage in all the hybrids.The five genes downstream of the circadian clock,and involved in chlorophyll and starch metabolic pathways,were expressed in AHP in hybrids with strong better-parent heterosis(BPH).Similarly,three of these Research Arfive genes in the japonica-japonica F1 hybrids showing low BPH were expressed in positive overdominance,but the other two genes were expressed in additive or negative overdominance.These results indicated that the expression patterns of circadian clock genes and their downstream genes are associated with heterosis,which suggests that the circadian rhythm pathway may be related to heterosis in rice.     

Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.)

In spite of commercial use of heterosis in agriculture, the molecular basis of heterosis is poorly understood. In this study, heterosis was estimated for eight root traits in 20 wheat hybrids derived from a NC Design II mating scheme. Positive mid-parent heterosis was detected in 96 of 160 hybrid–trait combinations, and positive high-parent heterosis was detected in 79 of 160 hybrid-trait combinations. Improved differential display was used to analyze alterations in gene expression between hybrids and their parents in roots at the jointing stage. More than 990 fragments were repeatedly displayed, among which 27.52% were differentially expressed between hybrids and their parents. Four differential expression patterns were observed. Thirty differentially expressed cDNA fragments and three genes with open reading frames were cloned, and their expression patterns were confirmed by reverse-northern blot and semi-quantitative RT-PCR analysis, respectively. We concluded that these differentially expressed genes, though mostly with unknown function, could play important roles for hybrids to demonstrate heterosis in root system traits.Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at .Z. Wang and Z. Ni contributed to this article equally.     

Genome‐wide identification and analysis of heterotic loci in three maize hybrids

Heterosis, or hybrid vigour, is a predominant phenomenon in plant genetics, serving as the basis of crop hybrid breeding, but the causative loci and genes underlying heterosis remain unclear in many crops. Here, we present a large‐scale genetic analysis using 5360 offsprings from three elite maize hybrids, which identifies 628 loci underlying 19 yield‐related traits with relatively high mapping resolutions. Heterotic pattern investigations of the 628 loci show that numerous loci, mostly with complete–incomplete dominance (the major one) or overdominance effects (the secondary one) for heterozygous genotypes and nearly equal proportion of advantageous alleles from both parental lines, are the major causes of strong heterosis in these hybrids. Follow‐up studies for 17 heterotic loci in an independent experiment using 2225 F₂ individuals suggest most heterotic effects are roughly stable between environments with a small variation. Candidate gene analysis for one major heterotic locus (ub3) in maize implies that there may exist some common genes contributing to crop heterosis. These results provide a community resource for genetics studies in maize and new implications for heterosis in plants.     

Single-parent expression complementation contributes to phenotypic heterosis in maize hybrids

The dominance model of heterosis explains the superior performance of F₁-hybrids via the complementation of deleterious alleles by beneficial alleles in many genes. Genes active in one parent but inactive in the second lead to single-parent expression (SPE) complementation in maize (Zea mays L.) hybrids. In this study, SPE complementation resulted in approximately 700 additionally active genes in different tissues of genetically diverse maize hybrids on average. We established that the number of SPE genes is significantly associated with mid-parent heterosis (MPH) for all surveyed phenotypic traits. In addition, we highlighted that maternally (SPE_B) and paternally (SPE_X) active SPE genes enriched in gene co-expression modules are highly correlated within each SPE type but separated between these two SPE types. While SPE_B-enriched co-expression modules are positively correlated with phenotypic traits, SPE_X-enriched modules displayed a negative correlation. Gene ontology term enrichment analyses indicated that SPE_B patterns are associated with growth and development, whereas SPE_X patterns are enriched in defense and stress response. In summary, these results link the degree of phenotypic MPH to the prevalence of gene expression complementation observed by SPE, supporting the notion that hybrids benefit from SPE complementation via its role in coordinating maize development in fluctuating environments.

The number of single-parent expression complementation patterns is significantly associated with mid-parent heterosis for all surveyed phenotypic traits in maize.     

Genetic Components of Heterosis for Seedling Traits in an Elite Rice Hybrid Analyzed Using an Immortalized F_2 Population

Utilization of heterosis has greatly contributed to rice productivity in China and many Asian countries. Superior hybrids usually show heterosis at two stages: canopy development at vegetative stage and panicle development at reproductive stage resulting in heterosis in yield. Although the genetic basis of heterosis in rice has been extensively investigated, all the previous studies focused on yield traits at maturity stage. In this study, we analyzed the genetic basis of heterosis at seedling stage making use of an "immortalized F2" population composed of 105 hybrids produced by intercrossing recombinant inbred lines(RILs) from a cross between Zhenshan 97 and Minghui 63,the parents of Shanyou 63, which is an elite hybrid widely grown in China. Eight seedling traits, seedling height, tiller number, leaf number, root number, maximum root length, root dry weight, shoot dry weight and total dry weight, were investigated using hydroponic culture. We analyzed single-locus and digenic genetic effects at the whole genome level using an ultrahigh-density SNP bin map obtained by population re-sequencing. The analysis revealed large numbers of heterotic effects for seedling traits including dominance, overdominance and digenic dominance(epistasis) in both positive and negative directions. Overdominance effects were prevalent for all the traits, and digenic dominance effects also accounted for a large portion of the genetic effects. The results suggested that cumulative small advantages of the single-locus effects and two-locus interactions, most of which could not be detected statistically, could explain the genetic basis of seedling heterosis of the F_1 hybrid.     

Relationships of differential gene expression in leaves with heterosis and heterozygosity in a rice diallel cross

Using differential display analysis, we assessed the patterns of differential gene expression in hybrids relative to their parents in a diallel cross involving 8 elite rice lines. The analysis revealed several patterns of differential expression including: (1) bands present in one parent and F₁ but absent in the other parent, (2) bands observed in both parents but not in the F₁, (3) bands occurring in only one parent but not in the F₁ or the other parent, and, (4) bands detected only in the F₁ but in neither of the parents. Relationships between differential gene expression and heterosis and marker heterozygosity were evaluated using data for RFLPs, SSRs and a number of agronomic characters. The analysis showed that there was very little correlation between patterns of differential expression and the F₁ means for all six agronomic traits. Differentially expressed fragments that occurred only in one parent but not in the other parent or in F₁ in each of the respective crosses were positively correlated with heterosis and heterozygosity. And conversely, fragments that were detected in F₁s but in neither of the respective parents were negatively correlated with heterosis and heterozygosity. The remaining patterns of differential expression were not correlated with heterosis or heterozygosity. The relationships between the patterns of differential expression and heterosis observed in this study were not consistent with expectations based on dominance or overdominance hypotheses.     

The role of epistasis in the manifestation of heterosis: a systems-oriented approach

Heterosis is widely used in breeding, but the genetic basis of this biological phenomenon has not been elucidated. We postulate that additive and dominance genetic effects as well as two-locus interactions estimated in classical QTL analyses are not sufficient for quantifying the contributions of QTL to heterosis. A general theoretical framework for determining the contributions of different types of genetic effects to heterosis was developed. Additive x additive epistatic interactions of individual loci with the entire genetic background were identified as a major component of midparent heterosis. On the basis of these findings we defined a new type of heterotic effect denoted as augmented dominance effect di* that comprises the dominance effect at each QTL minus half the sum of additive x additive interactions with all other QTL. We demonstrate that genotypic expectations of QTL effects obtained from analyses with the design III using testcrosses of recombinant inbred lines and composite-interval mapping precisely equal genotypic expectations of midparent heterosis, thus identifying genomic regions relevant for expression of heterosis. The theory for QTL mapping of multiple traits is extended to the simultaneous mapping of newly defined genetic effects to improve the power of QTL detection and distinguish between dominance and overdominance.     

Genomic selection of purebred animals for crossbred performance in the presence of dominant gene action

Background

Genomic selection is an appealing method to select purebreds for crossbred performance. In the case of crossbred records, single nucleotide polymorphism (SNP) effects can be estimated using an additive model or a breed-specific allele model. In most studies, additive gene action is assumed. However, dominance is the likely genetic basis of heterosis. Advantages of incorporating dominance in genomic selection were investigated in a two-way crossbreeding program for a trait with different magnitudes of dominance. Training was carried out only once in the simulation.

Results

When the dominance variance and heterosis were large and overdominance was present, a dominance model including both additive and dominance SNP effects gave substantially greater cumulative response to selection than the additive model. Extra response was the result of an increase in heterosis but at a cost of reduced purebred performance. When the dominance variance and heterosis were realistic but with overdominance, the advantage of the dominance model decreased but was still significant. When overdominance was absent, the dominance model was slightly favored over the additive model, but the difference in response between the models increased as the number of quantitative trait loci increased. This reveals the importance of exploiting dominance even in the absence of overdominance. When there was no dominance, response to selection for the dominance model was as high as for the additive model, indicating robustness of the dominance model. The breed-specific allele model was inferior to the dominance model in all cases and to the additive model except when the dominance variance and heterosis were large and with overdominance. However, the advantage of the dominance model over the breed-specific allele model may decrease as differences in linkage disequilibrium between the breeds increase. Retraining is expected to reduce the advantage of the dominance model over the alternatives, because in general, the advantage becomes important only after five or six generations post-training.

Conclusion

Under dominance and without retraining, genomic selection based on the dominance model is superior to the additive model and the breed-specific allele model to maximize crossbred performance through purebred selection.     

Identification and characterization of a repertoire of genes differentially expressed in developing top ear shoots between a superior hybrid and its parental inbreds in Zea mays L.

Heterosis has been widely used in crop breeding and production; however, little is known about the genes controlling trait heterosis. The shortage of genes known to function in heterosis significantly limits our understanding of the molecular basis underlying heterosis. Here, we report 748 genes differentially expressed (DG) in the developing top ear shoots between a maize heterotic F₁ hybrid (Mo17 × B73) and its parental inbreds identified using maize microarrays containing 28,608 unigene features. Of the 748 DG, over 600 were new for the inbred and hybrid combination. The DG were enriched for 35 of the total 213 maize gene ontology (GO) terms, including those describing photosynthesis, respiration, DNA replication, metabolism, and hormone biosynthesis. From the DG, we identified six genes involved in glycolysis, three genes in the citrate cycle, and four genes in the C4-dicarboxylic acid cycle. We mapped 533 of the 748 DG to the maize B73 genome, 298 (55.9 %) of which mapped to the QTL intervals of 11 maize ear traits. Moreover, we compared the repertoire of the DG with that of 14-day seedlings of the same inbred and hybrid combination. Only approximately 5 % of the DG was shared between the two organs and developmental stages. Furthermore, we mapped 417 (55.7 %) of the 748 maize DG to the QTL intervals of 26 rice yield-related traits. Therefore, this study provides a repertoire of genes useful for identification of genes involved in maize ear trait heterosis and information for a better understanding of the molecular basis underlying heterosis in maize.