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Plants have evolved an elaborate transcriptional machinery dedicated to eliciting sequence-specific, chromatin-based gene silencing. Two Pol II-related, plant-specific RNA polymerases, named Pol IV and Pol V, collaborate with proteins of the RNA interference machinery to generate long and short noncoding RNAs involved in epigenetic regulation. As revealed by a variety of genetic, molecular, and genomic technologies, these RNAs are used extensively in plants to direct the establishment, spread, and removal of DNA cytosine methylation throughout their genomes. RNA-mediated chromatin-level silencing is increasingly implicated in development, stress responses, and natural epigenetic variation that may promote phenotypic diversity, physiological plasticity, and evolutionary change.