Active DNA demethylation contributes to RNA modification and non-coding RNA expression in tomato

DNA 5-methylcytosine (5mC) is referred to as the "fifth base" of DNA and plays a crucial role in many biological processes such as gene expression and genome stability. RNA N6-methyladenosine (m6A) is a widely prevalent epigenetic marker in eukaryotes, participating in various RNA regulatory mechanisms, including translation and mRNA stability. Both 5mC and m6A modifications are dynamically regulated. After these epigenetic marks are established, 5mC and m6A can be actively removed by DNA demethylases and RNA demethylases, respectively. In plants, active DNA demethylation is controlled by the ROS1/DEMETER family, which removes 5mC bases from the DNA backbone through the base excision repair pathway, resulting in single-nucleotide gaps that can be filled with unmethylated cytosine. The Arabidopsis ros1 mutant exhibits genome-wide DNA hypermethylation, leading to reduced expression of certain genes and transposable elements (TEs). Knockout or knockdown of the tomato ROS1 homolog, SlDML2, significantly delays fruit ripening due to DNA hypermethylation in the promoter regions of ripening regulatory genes, resulting in their silencing. In addition to controlling ripening, SlDML2 also plays roles in several other developmental processes, such as seed germination, leaf and flower development, and disease resistance.