Epigenomic regulation of flowering in apple: Insights from two contrasting cultivars

• ‘Qinguan’ and ‘Fuji’ have completely opposite axillary bud flowering behaviors. • DNA methylation plays an important role in the regulation of axillary bud flowering. • DNA methylation of genes in plant hormone synthesis contributes to axillary bud flowering. Flowering is a necessary condition and the basis for yield in the life cycle of woody fruit trees. Although there has been considerable interest in the regulatory mechanisms underlying floral induction and flowering, the associated epigenetic modifications remain poorly characterized. We identified genome-wide DNA methylation changes and the transcriptional responses in axillary buds of ‘Qinguan’ (QA) and ‘Fuji’ (FA) varieties with contrasted flowering behaviors. The DNA methylation levels were19.35, 62.96 and 17.68% for FA, and 19.64, 62.49 and 17.86% for QA in the CG, CHG and CHH contexts, respectively. The number of hypermethylated or hypomethylated DMRs in different regions contributed to significantly up/downregulated gene expression. DNA methylation can positively or negatively regulate gene expression depending on the CG, CHG and CHH contexts and their locations in different regions. Additionally, the huge differences in transcription of MIKC c -Type MADS-box genes, and multiple flowering genes in multiple flowering pathways (i.e., light, age, GA and sugar) by changing DNA methylation, contributed to contrasted flowering behaviors in both QA and FA. Specifically, the floral meristem identity genes (i.e., FT, LEAFY, AP1 and SOC1 ) were significantly higher expression in QA than FA, but the floral repressor (i.e., SVP, AGL15 , and AGL18 ) showed the opposite trend. Significant differences in multiple hormone levels were due to DEGs and their DMRs in their synthesis pathways, leading to both contrasted axillary bud outgrowth and flowering behaviors. These findings reflect the diversity in the epigenetic regulation of gene expression and may be helpful for elucidating the epigenetic regulatory mechanism underlying the axillary bud flowering in apple.