Transcriptional gene silencing controls transposons and other repetitive elements through RNA-directed DNA methylation (RdDM) and heterochromatin formation. A key component of the Arabidopsis RdDM pathway is ARGONAUTE4 (AGO4), which associates with siRNAs to mediate DNA methylation. Here, we show that AGO4 preferentially targets transposable elements embedded within promoters of protein-coding genes. We find that this pattern of AGO4 binding cannot be simply explained by the sequences of AGO4-bound siRNAs, but instead AGO4 binding to specific gene promoters is also mediated by long non-coding RNAs (lncRNAs) produced by RNA Polymerase V. lncRNA-mediated AGO4 binding to gene promoters directs asymmetric DNA methylation to these genomic regions and is involved in regulating the expression of targeted genes. Finally, AGO4-binding overlaps sites of DNA methylation affected by biotic stress response. Based on these findings, we propose that targets of AGO4-directed RdDM are regulatory units responsible for controlling gene expression under specific environmental conditions.
© 2012 The Authors. The Plant Journal © 2012 Blackwell Publishing Ltd