SlJMJ7 orchestrates tomato fruit ripening via crosstalk between H3K4me3 and DML2-mediated DNA demethylation

The ripening of fleshy fruits is a unique developmental process that Arabidopsis and rice lack. This process is driven by hormones and transcription factors. However, the critical and early regulators of fruit ripening are still poorly understood. Here, we revealed that SlJMJ7, an H3K4 demethylase, is a critical negative regulator of fruit ripening in tomato. Combined genome-wide transcription, binding sites, histone H3K4me3 and DNA methylation analyses demonstrated that SlJMJ7 regulates a key group of ripening-related genes, including ethylene biosynthesis (ACS2, ACS4 and ACO6), transcriptional regulation (RIN and NOR) and DNA demethylation (DML2) genes, by H3K4me3 demethylation. Moreover, loss of SlJMJ7 function leads to increased H3K4me3 levels, which directly activates ripening-related genes, and to global DML2-mediated DNA hypomethylation in fruit, which indirectly prompts expression of ripening-related genes. Together, these effects lead to accelerated fruit ripening in sljmj7 mutant. Our findings demonstrate that SlJMJ7 acts as a master negative regulator of fruit ripening not only through direct removal of H3K4me3 from multiple key ripening-related factors, but also through crosstalk between histone and DNA demethylation. These findings reveal a novel crosstalk between histone methylation and DNA methylation to regulate gene expression in plant developmental processes.