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Cytosine DNA methylation protects eukaryotic genomes by silencing transposons and harmful DNAs, but also regulates gene expression during normal development. Loss of CG methylation in the  Arabidopsis thaliana met1  and  ddm1  mutants causes varied and stochastic developmental defects that are often inherited independently of the original  met1  or  ddm1  mutation. Loss of non-CG methylation in plants with combined mutations in the  DRM  and  CMT3  genes also causes a suite of developmental defects. We show here that the pleiotropic developmental defects of  drm1 drm2 cmt3  triple mutant plants are fully recessive, and unlike phenotypes caused by  met1  and  ddm1,  are not inherited independently of the  drm  and  cmt3  mutations. Developmental phenotypes are also reversed when  drm1 drm2 cmt3  plants are transformed with  DRM2  or  CMT3,  implying that non-CG DNA methylation is efficiently re-established by sequence-specific signals. We provide evidence that these signals include RNA silencing though the 24-nucleotide short interfering RNA (siRNA) pathway as well as histone H3K9 methylation, both of which converge on the putative chromatin-remodeling protein DRD1. These signals act in at least three partially intersecting pathways that control the locus-specific patterning of non-CG methylation by the DRM2 and CMT3 methyltransferases. Our results suggest that non-CG DNA methylation that is inherited via a network of persistent targeting signals has been co-opted to regulate developmentally important genes.

RNAi, DRD1, and Histone Methylation Actively Target Developmentally Important Non-CG DNA Methylation in Arabidopsis