Nonadditive gene expression contributing to heterosis in partially heterozygous maize hybrids is predominantly regulated from heterozygous regions

Hybrids often perform better than their homozygous parents, a phenomenon that is commonly referred to as heterosis. Heterosis is widely utilized in modern agriculture, although its molecular basis is not very well understood. In this study, we backcrossed an intermated recombinant inbred line population of maize (Zea mays L.) with its parental inbred lines B73 and Mo17. The resulting hybrids exhibited different degrees of heterozygosity and heterosis. We identified nonadditively expressed genes, which are expressed differently from their mid-parental level. In addition, we surveyed their regulation by investigating expression quantitative trait loci (eQTL). Nonadditively expressed genes explain up to 27% of heterotic variance in the backcross hybrids. Furthermore, nonadditively expressed genes are regulated almost exclusively from heterozygous regions of the genome. We observed that nonadditive expression patterns are distinctly regulated depending on the genetic origin of the higher expressed parent. As a consequence, these regulatory regimes lead to higher gene activity in most nonadditively expressed genes in the hybrids. We demonstrated that nonadditive expression patterns contribute to heterosis and their mode of regulation might translate phylogenetic distance into vigorous hybrids. Based on our results, we hypothesize that diverging regulatory preferences in inbred lines are beneficial for selecting parental combinations for hybrid breeding.