Local and global crosstalk among heterochromatin marks drives DNA methylome patterning in Arabidopsis

In plant genomes, both mCG and H3K9me2/mCH are important for silencing transposable elements (TEs). Here, the authors show that establishment of mCH is abolished in both TE and active genes when mCG is lost and targeting efficiency of mCH depends on relative levels of mCG within the genome. Transposable elements (TEs) are robustly silenced by multiple epigenetic marks, but dynamics of crosstalk among these marks remains enigmatic. In Arabidopsis, TEs are silenced by cytosine methylation in both CpG and non-CpG contexts (mCG and mCH) and histone H3 lysine 9 methylation (H3K9me). While mCH and H3K9me are mutually dependent for their maintenance, mCG and mCH/H3K9me are independently maintained. Here, we show that establishment, rather than maintenance, of mCH depends on mCG, accounting for the synergistic colocalization of these silent marks in TEs. When mCG is lost, establishment of mCH is abolished in TEs. mCG also guides mCH in active genes, though the resulting mCH/H3K9me is removed thereafter. Unexpectedly, targeting efficiency of mCH depends on relative, rather than absolute, levels of mCG within the genome, suggesting underlying global negative controls. We propose that local positive feedback in heterochromatin dynamics, together with global negative feedback, drive robust and balanced DNA methylome patterning.

Automated summary

In plant genomes, both mCG and H3K9me2/mCH play important roles in silencing TEs. The establishment of mCH is dependent on the presence of mCG, and the efficiency of mCH targeting depends on the relative levels of mCG in the genome. The study also proposes a model where local positive feedback and global negative feedback regulate DNA methylation patterning.