Epigenomic Regulatory Mechanism in Vegetative Phase Transition of Malus hupehensis

In woody plants, phase transitions substantially affect growth and development. Although there has been considerable interest in the regulatory mechanisms underlying phase changes, the associated epigenetic modifications remain relatively uncharacterized. We examined the DNA methylation changes and the transcriptional responses in adult and juvenile Malus hupehensis leaves. The DNA methylations were 66.61% and 68.3% in the CG context, 49.12% and 52.44% in the CHG context, and 7.02% and 8.22% in the CHH context for the adult and juvenile leaves, respectively. The number of differentially methylated regions in all contexts distributed in the genic regions varied. Additionally, inhibited DNA methylation in adult leaves activated the transcription of indole-3-acetic acid related genes in the signaling, response, and transport pathways. Moreover, the opposite methylation and expression patterns were observed for the SPL and AP2 family genes between the adult and juvenile leaves. Both gene families contribute to the M. hupehensis vegetative phase transition. Furthermore, the hyper-/hypomethylation of the gene body or promoter of transcription factor genes may lead to up-/downregulated gene expression. The methylation levels of the WRKY (22), NAC (21), ERF (8), WOX (2), KNAT (6), EIN3 (2), SCL (7), ZAT (7), and HSF (4) genes were higher in the adult leaves than in the juvenile leaves, whereas the opposite pattern was observed for the TCP (2), MADS-box (11), and DOF (3) genes. An analysis of the correlation between methylation and transcription indicated the methylation of the gene body in all contexts and the methylation of the promoter in the CG and CHG contexts are negatively correlated with gene expression. However, the methylation of the promoter in the CHH context is positively correlated with gene expression. These findings reflect the diversity in the epigenetic regulation of gene expression and may be useful for elucidating the epigenetic regulatory mechanism underlying the M. hupehensis vegetative phase transition.