Histone modification H3K27me3 is essential during chilling-induced flowering in Litchi chinensis

Abstract Litchi (Litchi chinensis), a prominent fruit tree in the Sapindaceae, initiates flowering in response to low autumn and winter temperatures. This study investigates the epigenetic regulation of this process, focusing on the marks histone H3 lysine 27 trimethylation (H3K27me3) and its deposition genes during the chilling-induced floral induction and initiation stages. Our genomic analysis delineated the H3K27me3 deposition landscape across the pre-floral induction (PFId), floral induction (FId), and floral initiation (FIn) stages. We identified 5,635 differentially H3K27me3-modified genes (DHGs) in buds and 4,801 DHGs in leaves. Integration of the RNA-seq and ChIP-seq datasets identified 1,001 differentially regulated genes (DRGs) in buds and 675 DRGs in leaves, offering insights into the genes potentially targeted by H3K27me3. To probe the functional role of H3K27me3, we employed GSK343, a histone H3 lysine methyltransferase inhibitor. Treatment with GSK343 during the chilling-induced flowering process led to reduced H3K27me3 deposition at the TREHALOSE-6-PHOSPHATE SYNTHASE 1 (LcTPS1) and FRIGIDA (LcFRI) loci, resulting in increased gene expression. This manipulation delayed flowering and reduced flowering rates, confirming the pivotal role of H3K27me3 in chilling-induced flowering in litchi. Gene co-expression network analysis identified SHORT VEGETATIVE PHASE 10 (LcSVP10) as a crucial regulator in litchi flowering. Overexpression of LcSVP10 in Arabidopsis thaliana delayed flowering, indicating a conserved function in flowering time control. Our results elucidate the molecular and epigenetic mechanisms that govern floral induction in litchi and highlight the potential of epigenetic modifications to regulate flowering time in horticultural plants.