Eukaryotic DNA cytosine methylation can be used to transcriptionally silence 
repetitive sequences, including transposons and retroviruses. This silencing is 
stable between cell generations as cytosine methylation is maintained 
epigenetically through DNA replication. The Arabidopsis thaliana Dnmt3 cytosine 
methyltransferase ortholog DOMAINS rearranged methyltransferase2 (DRM2) is 
required for establishment of small interfering RNA (siRNA) directed DNA 
methylation. In mammals PIWI proteins and piRNA act in a convergently evolved 
RNA-directed DNA methylation system that is required to repress transposon 
expression in the germ line. De novo methylation may also be independent of RNA 
interference and small RNAs, as in Neurospora crassa. Here we identify a clade 
of catalytically mutated DRM2 paralogs in flowering plant genomes, which in 
A.thaliana we term domains rearranged methyltransferase3 (DRM3). Despite being 
catalytically mutated, DRM3 is required for normal maintenance of non-CG DNA 
methylation, establishment of RNA-directed DNA methylation triggered by repeat 
sequences and accumulation of repeat-associated small RNAs. Although the 
mammalian catalytically inactive Dnmt3L paralogs act in an analogous manner, 
phylogenetic analysis indicates that the DRM and Dnmt3 protein families diverged 
independently in plants and animals. We also show by site-directed mutagenesis 
that both the DRM2 N-terminal UBA domains and C-terminal methyltransferase 
domain are required for normal RNA-directed DNA methylation, supporting an 
essential targeting function for the UBA domains. These results suggest that 
plant and mammalian RNA-directed DNA methylation systems consist of a 
combination of ancestral and convergent features.