Reciprocal Genetics: Identifying QTL for General and Specific Combining Abilities in Hybrids Between Multiparental Populations from Two Maize (Zea mays L.) Heterotic Groups.

Several plant and animal species of agricultural importance are commercialized as hybrids to take advantage of the heterosis phenomenon. Understanding the genetic architecture of hybrid performances is therefore of key importance. We developed two multiparental maize (Zea mays L.) populations, each corresponding to an important heterotic group (dent or flint) and comprised of six connected biparental segregating populations of inbred lines (802 and 822 lines for each group, respectively) issued from four founder lines. Instead of using "testers" to evaluate their hybrid values, segregating lines were crossed according to an incomplete factorial design to produce 951 dent-flint hybrids, evaluated for four biomass production traits in eight environments. QTL detection was carried out for the general-combining-ability (GCA) and specific-combining-ability (SCA) components of hybrid value, considering allelic effects transmitted from each founder line. In total, 42 QTL were detected across traits. We detected mostly QTL affecting GCA, 31% (41% for dry matter yield) of which also had mild effects on SCA. The small impact of dominant effects is consistent with the known differentiation between the dent and flint heterotic groups and the small percentage of hybrid variance due to SCA observed in our design (∼20% for the different traits). Furthermore, most (80%) of GCA QTL were segregating in only one of the two heterotic groups. Relative to tester-based designs, use of hybrids between two multiparental populations appears highly cost efficient to detect QTL in two heterotic groups simultaneously. This presents new prospects for selecting superior hybrid combinations with markers.

Linkage Analysis and Association Mapping QTL Detection Models for Hybrids Between Multiparental Populations from Two Heterotic Groups: Application to Biomass Production in Maize (Zea mays L.).

Identification of quantitative trait loci (QTL) involved in the variation of hybrid value is of key importance for cross-pollinated species such as maize (Zea mays L.). In a companion paper, we illustrated a new QTL mapping population design involving a factorial mating between two multiparental segregating populations. Six biparental line populations were developed from four founder lines in the Dent and Flint heterotic groups. They were crossed to produce 951 hybrids and evaluated for silage performances. Previously, a linkage analysis (LA) model that assumes each founder line carries a different allele was used to detect QTL involved in General and Specific Combining Abilities (GCA and SCA, respectively) of hybrid value. This previously introduced model requires the estimation of numerous effects per locus, potentially affecting QTL detection power. Using the same design, we compared this "Founder alleles" model to two more parsimonious models, which assume that (i) identity in state at SNP alleles from the same heterotic group implies identity by descent (IBD) at linked QTL ("SNP within-group" model) or (ii) identity in state implies IBD, regardless of population origin of the alleles ("Hybrid genotype" model). This last model assumes biallelic QTL with equal effects in each group. It detected more QTL on average than the two other models but explained lower percentages of variance. The "SNP within-group" model appeared to be a good compromise between the two other models. These results confirm the divergence between the Dent and Flint groups. They also illustrate the need to adapt the QTL detection model to the complexity of the allelic variation, which depends on the trait, the QTL, and the divergence between the heterotic groups.

Dearth of polymorphism associated with a sustained response to selection for flowering time in maize.

BACKGROUND: Long term selection experiments bring unique insights on the genetic architecture of quantitative traits and their evolvability. Indeed, they are utilized to (i) monitor changes in allele frequencies and assess the effects of genomic regions involved traits determinism; (ii) evaluate the role of standing variation versus new mutations during adaptation; (iii) investigate the contribution of non allelic interactions. Here we describe genetic and phenotypic evolution of two independent Divergent Selection Experiments (DSEs) for flowering time conducted during 16 years from two early maize inbred lines. RESULTS: Our experimental design uses selfing as the mating system and small population sizes, so that two independent families evolved within each population, Late and Early. Observed patterns are strikingly similar between the two DSEs. We observed a significant response to selection in both directions during the first 7 generations of selection. Within Early families, the response is linear through 16 generations, consistent with the maintenance of genetic variance. Within Late families and despite maintenance of significant genetic variation across 17 generations, the response to selection reached a plateau after 7 generations. This plateau is likely caused by physiological limits. Residual heterozygosity in the initial inbreds can partly explain the observed responses as evidenced by 42 markers derived from both Methyl-Sensitive Amplification- and Amplified Fragment Length- Polymorphisms. Among the 42, a subset of 13 markers most of which are in high linkage disequilibrium, display a strong association with flowering time variation. Their fast fixation throughout DSEs' pedigrees results in strong genetic differentiation between populations and families. CONCLUSIONS: Our results reveal a paradox between the sustainability of the response to selection and the associated dearth of polymorphisms. Among other hypotheses, we discuss the maintenance of heritable variation by few mutations with strong epistatic interactions whose effects are modified by continuous changes of the genetic background through time.

Flowering time in maize: linkage and epistasis at a major effect locus.

In a previous study, we identified a candidate fragment length polymorphism associated with flowering time variation after seven generations of selection for flowering time, starting from the maize inbred line F252. Here, we characterized the candidate region and identified underlying polymorphisms. Then, we combined QTL mapping, association mapping, and developmental characterization to dissect the genetic mechanisms responsible for the phenotypic variation. The candidate region contained the Eukaryotic Initiation Factor (eIF-4A) and revealed a high level of sequence and structural variation beyond the 3'-UTR of eIF-4A, including several insertions of truncated transposable elements. Using a biallelic single-nucleotide polymorphism (SNP) (C/T) in the candidate region, we confirmed its association with flowering time variation in a panel of 317 maize inbred lines. However, while the T allele was correlated with late flowering time within the F252 genetic background, it was correlated with early flowering time in the association panel with pervasive interactions between allelic variation and the genetic background, pointing to underlying epistasis. We also detected pleiotropic effects of the candidate polymorphism on various traits including flowering time, plant height, and leaf number. Finally, we were able to break down the correlation between flowering time and leaf number in the progeny of a heterozygote (C/T) within the F252 background consistent with causal loci in linkage disequilibrium. We therefore propose that both a cluster of tightly linked genes and epistasis contribute to the phenotypic variation for flowering time.

The genetic architecture of grain yield and related traits in Zea maize L. revealed by comparing intermated and conventional populations.

Using advanced intermated populations has been proposed as a way to increase the accuracy of mapping experiments. An F(3) population of 300 lines and an advanced intermated F(3) population of 322 lines, both derived from the same parental maize inbred lines, were jointly evaluated for dry grain yield (DGY), grain moisture (GM), and silking date (SD). Genetic variance for dry grain yield was significantly lower in the intermated population compared to the F(3) population. The confidence interval around a QTL was on average 2.31 times smaller in the intermated population compared to the F(3) population. One controversy surrounding QTL mapping is whether QTL identified in fact represent single loci. This study identifies two distinct loci for dry grain yield in the intermated population in coupling phase, while the F(3) identifies only a single locus. Surprisingly, fewer QTL were detected in the intermated population than the F(3) (21 vs. 30) and <50% of the detected QTL were shared among the two populations. Cross-validation showed that selection bias was more important in the intermated population than in the F(3) and that each detected QTL explained a lower percentage of the variance. This finding supports the hypothesis that QTL detected in conventional populations correspond mainly to clusters of linked QTL. The actual number of QTL involved in the genetic architecture of complex traits may be substantially larger, with effect sizes substantially smaller than in conventional populations.

Standing variation and new mutations both contribute to a fast response to selection for flowering time in maize inbreds.

BACKGROUND: In order to investigate the rate and limits of the response to selection from highly inbred genetic material and evaluate the respective contribution of standing variation and new mutations, we conducted a divergent selection experiment from maize inbred lines in open-field conditions during 7 years. Two maize commercial seed lots considered as inbred lines, F252 and MBS847, constituted two biological replicates of the experiment. In each replicate, we derived an Early and a Late population by selecting and selfing the earliest and the latest individuals, respectively, to produce the next generation. RESULTS: All populations, except the Early MBS847, responded to selection despite a short number of generations and a small effective population size. Part of the response can be attributed to standing genetic variation in the initial seed lot. Indeed, we identified one polymorphism initially segregating in the F252 seed lot at a candidate locus for flowering time, which explained 35% of the trait variation within the Late F252 population. However, the model that best explained our data takes into account both residual polymorphism in the initial seed lots and a constant input of heritable genetic variation by new (epi)mutations. Under this model, values of mutational heritability range from 0.013 to 0.025, and stand as an upper bound compare to what is reported in other species. CONCLUSIONS: Our study reports a long-term divergent selection experiment for a complex trait, flowering time, conducted on maize in open-field conditions. Starting from a highly inbred material, we created within a few generations populations that strikingly differ from the initial seed lot for flowering time while preserving most of the phenotypic characteristics of the initial inbred. Such material is unique for studying the dynamics of the response to selection and its determinants. In addition to the fixation of a standing beneficial mutation associated with a large phenotypic effect, a constant input of genetic variance by new mutations has likely contributed to the response. We discuss our results in the context of the evolution and mutational dynamics of populations characterized by a small effective population size.

Fine mapping and haplotype structure analysis of a major flowering time quantitative trait locus on maize chromosome 10.

Flowering time is a major adaptive trait in plants and an important selection criterion for crop species. In maize, however, little is known about its molecular basis. In this study, we report the fine mapping and characterization of a major quantitative trait locus located on maize chromosome 10, which regulates flowering time through photoperiod sensitivity. This study was performed in near-isogenic material derived from a cross between the day-neutral European flint inbred line FV286 and the tropical short-day inbred line FV331. Recombinant individuals were identified among a large segregating population and their progenies were scored for flowering time. Combined genotypic characterization led to delimit the QTL to an interval of 170 kb and highlighted an unbalanced recombination pattern. Two bacterial artificial chromosomes (BACs) covering the region were analyzed to identify putative candidate genes, and synteny with rice, sorghum, and brachypodium was investigated. A gene encoding a CCT domain protein homologous to the rice Ghd7 heading date regulator was identified, but its causative role was not demonstrated and deserves further analyses. Finally, an association study showed a strong level of linkage disequilibrium over the region and highlighted haplotypes that could provide useful information for the exploitation of genetic resources and marker-assisted selection in maize.