The genetic basis of heterosis: multiparental quantitative trait loci mapping reveals contrasted levels of apparent overdominance among traits of agronomical interest in maize (Zea mays L.)

Abstract

Understanding the genetic bases underlying heterosis is a major issue in maize (Zea mays L.). We extended the North Carolina design III (NCIII) by using three populations of recombinant inbred lines derived from three parental lines belonging to different heterotic pools, crossed with each parental line to obtain nine families of hybrids. A total of 1253 hybrids were evaluated for grain moisture, silking date, plant height, and grain yield. Quantitative trait loci (QTL) mapping was carried out on the six families obtained from crosses to parental lines following the "classical" NCIII method and with a multiparental connected model on the global design, adding the three families obtained from crosses to the nonparental line. Results of the QTL detection highlighted that most of the QTL detected for grain yield displayed apparent overdominance effects and limited differences between heterozygous genotypes, whereas for grain moisture predominance of additive effects was observed. For plant height and silking date results were intermediate. Except for grain yield, most of the QTL identified showed significant additive-by-additive epistatic interactions. High correlation observed between heterosis and the heterozygosity of hybrids at markers confirms the complex genetic basis and the role of dominance in heterosis. An important proportion of QTL detected were located close to the centromeres. We hypothesized that the lower recombination in these regions favors the detection of (i) linked QTL in repulsion phase, leading to apparent overdominance for heterotic traits and (ii) linked QTL in coupling phase, reinforcing apparent additive effects of linked QTL for the other traits.

Figure 1

Correlation between augmented dominance effect (Z₂) and modified Rogers distance (MRD²) to parent 1 for all the studied traits [grain moisture (%), silking date (days), plant height (cm), and grain yield (q ⋅ ha⁻¹)]. Population D stands for the population deriving from the cross of the parental lines F2 and Io. Population E stands for the population deriving from F2 and F252 and population G stands for the population deriving from Io × F252.

Figure 2

QTL projection for the global design (Trait) and the three NCIII designs (Z₁ and Z₂) for grain moisture, silking date, plant height, and grain yield. Each QTL is displayed by one horizontal line bound by two vertical lines representing the confidence interval and a vertical line proportional to the QTL R² symbolizing the QTL position. The solid triangle points to the approximate centromere position.

Figure3

Genetic effects for some representative QTL detected on the global design for grain moisture (%), silking date (days), plant height (cm), and grain yield (q ⋅ ha⁻¹). Homozygous genotypes are represented by solid circles, and heterozygous genotypes are represented by crosses. Triangle sides join homozygous genotypes whereas vertical lines represent the deviation of each heterozygous genotype from the average of corresponding homozygous genotypes (i.e., dominance effect). 1 indicates the F2 allele, 2 the Io allele, and 3 the F252 allele.