Epistasis Activation Contributes Substantially to Heterosis in Temperate by Tropical Maize Hybrids

Epistasis strongly affects the performance of superior maize hybrids. In this study, a multiple-hybrid population, consisting of three hybrid maize sets with varied interparental divergence, was generated by crossing 28 temperate and 23 tropical inbred lines with diverse genetic backgrounds. We obtained 1,154 tested hybrids. Among these tested hybrids, heterosis increased steadily as the heterotic genetic distance increased. Mid-parent heterosis was significantly higher in the temperate by tropical hybrids than in the temperate by temperate hybrids. Genome-wide prediction and association mapping was performed for grain weight per plant (GWPP) and days to silking (DTS) using 20K high-quality SNPs, showing that epistatic effects played a more prominent role than dominance effects in temperate by tropical maize hybrids. A total of 33 and 420 epistatic QTL were identified for GWPP and DTS, respectively, in the temperate by tropical hybrids. Protein-protein interaction network and gene-set enrichment analyses showed that epistatic genes were involved in protein interactions, which play an important role in photosynthesis, biological transcription pathways, and protein synthesis. We showed that the interaction of many minor-effect genes in the hybrids could activate the transcription activators of epistatic genes, resulting in a cascade of amplified yield heterosis. The multiple-hybrid population design enhanced our understanding of heterosis in maize, providing an insight into the acceleration of hybrid maize breeding by activating epistatic effects.