RNA polymerase V targets transcriptional silencing components to promoters of protein‐coding genes

Summary Transcriptional gene silencing controls transposons and other repetitive elements through RNA ‐directed DNA methylation ( R d DM ) and heterochromatin formation. A key component of the Arabidopsis R d DM pathway is ARGONAUTE 4 ( AGO 4), which associates with siRNAs to mediate DNA methylation. Here, we show that AGO 4 preferentially targets transposable elements embedded within promoters of protein‐coding genes. This pattern of AGO 4 binding cannot be simply explained by the sequences of AGO 4‐bound si RNA s; instead, AGO 4 binding to specific gene promoters is also mediated by long non‐coding RNA s (lnc RNA s) produced by RNA polymerase V . lnc RNA ‐mediated AGO 4 binding to gene promoters directs asymmetric DNA methylation to these genomic regions and is involved in regulating the expression of targeted genes. Finally, AGO 4 binding overlaps sites of DNA methylation affected by the biotic stress response. Based on these findings, we propose that the targets of AGO 4‐directed R d DM are regulatory units responsible for controlling gene expression under specific environmental conditions.