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Abstract In mammals and plants, cytosine DNA methylation is essential for the epigenetic repression of transposable elements and foreign DNA. In plants, DNA methylation is guided by small interfering RNAs (siRNAs) in a self-reinforcing cycle termed RNA-directed DNA methylation (RdDM). RdDM requires the specialized RNA polymerase V (Pol V), and the key unanswered question is how Pol V is first recruited to new target sites without pre-existing DNA methylation. We find that Pol V follows and is dependent on the recruitment of an AGO4-clade ARGONAUTE protein, and any siRNA can guide the ARGONAUTE protein to the new target locus independent of pre-existing DNA methylation. These findings reject long-standing models of RdDM initiation and instead demonstrate that siRNA-guided ARGONAUTE targeting is necessary, sufficient and first to target Pol V recruitment and trigger the cycle of RdDM at a transcribed target locus, thereby establishing epigenetic silencing. 

Summary Plant responses to abiotic environmental challenges are known to have lasting effects on the plant beyond the initial stress exposure. Some of these lasting effects are transgenerational, affecting the next generation. The plant response to elevated carbon dioxide (CO₂) levels has been well studied. However, these investigations are typically limited to plants grown for a single generation in a high CO₂environment while transgenerational studies are rare.We aimed to determine transgenerational growth responses in plants after exposure to high CO₂by investigating the direct progeny when returned to baseline CO₂levels.We found that both the flowering plantArabidopsis thalianaand seedless nonvascular plantPhyscomitrium patenscontinue to display accelerated growth rates in the progeny of plants exposed to high CO₂. We used the model species Arabidopsis to dissect the molecular mechanism and found that DNA methylation pathways are necessary for heritability of this growth response.More specifically, the pathway of RNA‐directed DNA methylation is required to initiate methylation and the proteins CMT2 and CMT3 are needed for the transgenerational propagation of this DNA methylation to the progeny plants. Together, these two DNA methylation pathways establish and then maintain a cellular memory to high CO₂exposure.