Transcriptome dynamics and allele-specific regulation underlie wheat heterosis at the anthesis and grain-filling stages

Abstract

Abstract Background As wheat is a globally important staple crop, the molecular regulatory network underlying heterosis in wheat remains incompletely understood. The flag leaf is the primary source of photoassimilates during grain filling and plays a crucial role in yield formation. However, the genetic mechanisms linking flag leaf development to heterosis are still unclear. Results Transcriptomic analysis revealed dynamic transcriptional reprogramming during the anthesis to grain-filling transition, with a pronounced expression bias toward superior parental alleles in hybrids. Anthesis-stage non-additive dominance and grain-filling-stage additive enhancement synergistically orchestrated the temporal regulatory shift underlying heterosis. The dominant alleles from the superior parent accounted for more than 60% of the non-additive genes, and the superior parent bias in allele-specific expression ratios progressively increased during development. This highlighted the role of the superior parent as an allelic reservoir. Cis-regulatory variations primarily contributed to additive effects, whereas cis×trans interactions were the primary regulatory driver of positive overdominance. Notably, weighted co-expression network analysis identified HSP90.2-B as a putative heterosis-related gene, whose coordinated overexpression with AP2/ERF transcription factors provides valuable insights for elucidating the molecular basis of yield heterosis. Conclusions This study establishes two complementary models to decode the molecular regulation of heterosis in wheat. The “dual-engine” model demonstrates stage-specific gene expression patterns: non-additive effects predominantly drive early growth vigor during the anthesis stage, whereas additive expression patterns stabilize grain development and yield-related traits at the grain-filling stage. The “two-phase regulatory shift” model captures the dynamic temporal progression of heterotic regulation, evolving from trans-regulation-driven plastic responses at the anthesis stage to cis-regulation-mediated homeostatic control at the grain-filling stage. Importantly, the preferential coupling between cis-regulation/additive and trans-regulation/non-additive expression provides molecular evidence supporting the complementary nature of the models. We further identified developmentally specific modules (the anthesis-stage Red module and grain-filling-stage Brown module) with their core regulatory networks through weighted gene co-expression network analysis. These findings preliminarily characterize the multi-layered cooperative networks regulating heterosis development, potentially offering valuable theoretical clues for deciphering the molecular mechanisms underlying wheat heterosis.

Keywords

• Triticum aestivum L.
• Heterosis
• Transcriptome
• Allele-specific expression
• Additive and non-additive expression patterns
• Cis- and trans-regulation