Gen Xu, Xuerong Yang, Mingyue Zhang, Congbin Kang, Ziang Tian, Yunhui Qi, Meijie Luo, Peng Liu, Jeffrey Ross-Ibarra, Jinliang Yang, Hongjun Liu
Heterosis, or hybrid vigor, is a key genetic and agricultural phenomenon driven by non-additive effects, though its mechanisms remain debated. To examine these effects at the transcriptomic level, we integrate population-scale transcriptomic and phenotypic data in maize. We find that ∼30% of expressed seedling genes in many hybrids deviate from mid-parent values, consistent with incomplete dominance. While overall expression is largely controlled by cis-eQTLs, non-additive expression is disproportionately regulated by trans-eQTLs. These trans-eQTLs cluster into hotspots that coordinately control hundreds of genes, often within co-expression networks and enriched for transcription factors. We validate one hotspot involving ZmR1, a bHLH transcription factor, showing its role in regulating widespread incomplete dominance and enhancing heterosis in seedling and agronomic traits. These findings support a model in which trans-acting factors shape expression dominance and contribute to heterosis, providing a framework for crop improvement. This study shows that maize hybrids exhibit increased transcriptome activity than inbred parents in an incomplete dominance manner, contributing to hybrid vigor. This increase is primarily regulated by transcription factors acting as trans-eQTLs.