The incomplete dominance of gene expression controlled by Trans-eQTL hotspots contributes to heterosis in maize.

Abstract

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.