Dynamics of Gene and Allelic Expression During Modern Hybrid Maize Breeding

Maize breeding has greatly improved yield through single-cross hybrids, but the underlying gene regulatory changes remain unclear. This study analysed transcriptomes of landmark maize hybrids and their parents across developmental stages and planting densities. Compared with their parents, hybrids showed a trade-off in the expression of photosynthesis-related genes and stress-responsive genes. This expression rebalancing suggested a strategy that prioritises photosynthetic efficiency and growth vigour over stress defence mechanisms. Allele-specific expression (ASE) analysis identified 19.9% of heterozygous loci exhibiting significant allelic imbalance, with notable enrichment in photosynthesis and stress response pathways. Importantly, the suppressed expression of deleterious alleles in hybrids not only correlated with phenotypic performance but also exhibited progressive enhancement through decades of breeding, indicating this regulatory mechanism has been selected during improvement. Consistent with this finding, breeding selection preferentially acted on cis-regulatory regions, with stronger correlation between cis-regulatory complementation of deleterious variants and hybrid release year compared to coding regions. Transcriptomic plasticity across environments was evaluated using the concept of entropy. Results showed that hybrids had lower transcriptomic entropy than their parental lines, and this reduction in entropy was significantly associated with heterosis. These findings highlight the critical role of allelic expression optimization in maize hybrid breeding and provide insights into the transcriptomic dynamics that underlie heterosis.