Histone methyltransferase BnaSUVH1 drives photosynthesis and biomass heterosis via expression level dominance (ELD) in Brassica napus

Abstract Utilization of heterosis is a critical and successful strategy for increasing crop yields. Although epigenetic regulation has been implicated in heterosis, its precise regulatory patterns and networks remain unclear. To explore the underlying epigenetic mechanisms, the elite rapeseed hybrid cultivar Fengyou 737 (FY737) and its parental lines were used. The hybrid FY737 showed remarkable heterosis in both photosynthesis and biomass at the vegetative stage. To investigate the molecular basis, we performed whole-transcriptome sequencing, and differentially expressed (DE) mRNAs, lncRNAs and miRNAs were identified. Analysis of these expression patterns (additivity, ELD and transgressive regulation) revealed that more than 80% of DE transcripts displayed an ELD effect. Notably, a competing endogenous RNA (ceRNA) network lncBnaMEFG2-novel_miR_187-BnaSUVH1 (SU(VAR)3–9 HOMOLOG 1) was specifically associated with ELD-F (female) effect. SUVH1 is a histone methyltransferase that catalyzes H3 lysine 4 trimethylation (H3K4me3) and typically binds methylated DNA regions to activate downstream targets. Integration of DNA methylation and H3K4me3 profiles revealed that BnaSUVH1 epigenetically activates a suite of downstream targets, including key light-responsive proteins, a photoreceptor, two photoregulatory protein kinases, and a Mn/Ca transporter. Consistently, Bnasuvh1 CRISPR-Cas9 knockout mutants exhibited significantly reduced biomass and photosynthetic efficiency compared with the wild-type plants, confirming the causal role of BnaSUVH1 in heterosis. These findings demonstrate that the ceRNA network lncBnaMEFG2-novel_miR_187-BnaSUVH1 promotes heterosis by fine-tuning the epigenetic activation of light-responsive and photosynthetic genes. Our study provides novel insights into the epigenetic basis of heterosis and supports future high-yield breeding in rapeseed.