Pathway conversion enables a double-lock mechanism to maintain DNA methylation and genome stability.

The CMT2 and RNA-directed DNA methylation (RdDM) pathways have been proposed to separately maintain CHH methylation in specific regions of the Arabidopsis thaliana genome. Here, we show that dysfunction of the chromatin remodeler DDM1 causes hundreds of genomic regions to switch from CMT2 dependency to RdDM dependency in DNA methylation. These converted loci are enriched at the edge regions of long transposable elements (TEs). Furthermore, we found that dysfunction in both DDM1 and RdDM causes strong reactivation of TEs and a burst of TE transposition in the first generation of mutant plants, indicating that the DDM1 and RdDM pathways together are critical to maintaining TE repression and protecting genomic stability. Our findings reveal the existence of a pathway conversion–based backup mechanism to guarantee the maintenance of DNA methylation and genome integrity.