Plants repress ROS1 expression to attenuate heat-induced transposon burst

The active DNA demethylase Repressor of Silencing 1 (ROS1) regulates genomic DNA methylation patterns during plant development. ROS1 expression is promoted by DNA methylation within its promoter region. However, the mechanisms and biological significance of ROS1 regulation under abiotic stresses remain elusive. Here we show that heat stress reduces DNA methylation in the ROS1 promoter to suppress its expression. Under normal conditions, SUVH1 and SUVH3 bind methylated ROS1 promoter regions, inhibiting chromatin interactions around the ROS1 locus; heat stress triggers their dissociation, enabling chromatin loop formation to suppress ROS1 transcription. Transgenic plants with exogenous ROS1 maintain high expression levels during heat stress, causing transposable element hypomethylation and enhanced transcription and transgenerational transposition of the heat-activated retrotransposon ONSEN. We propose that heat-induced suppression of ROS1 transcription, which is conserved across plant species, serves as a brake system to limit transposable element activation, thereby safeguarding genome stability.