Fan Lingjiao, Jing Yuqing, Liu Xinyu, Zhang Wenxin, Mi Yingjie, Sun Linhua, Fan Liu-Min, Qian Weiqiang
State Key Laboratory of Wheat Improvement, School of Advanced Agricultural Sciences, Peking University, Beijing, China.
Beijing Life Science Academy, Beijing, China.
Nat Plants. 2025 Aug 11. doi: 10.1038/s41477-025-02076-9.
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.
活性DNA去甲基化酶沉默抑制因子1（ROS1）在植物发育过程中调节基因组DNA甲基化模式。ROS1的表达受其启动子区域内DNA甲基化的促进。然而，非生物胁迫下ROS1调控的机制和生物学意义仍不清楚。在这里，我们表明热胁迫会降低ROS1启动子中的DNA甲基化，从而抑制其表达。在正常条件下，SUVH1和SUVH3与甲基化的ROS1启动子区域结合，抑制ROS1基因座周围的染色质相互作用；热胁迫触发它们的解离，使染色质环形成，从而抑制ROS1转录。携带外源ROS1的转基因植物在热胁迫期间保持高表达水平，导致转座元件去甲基化，并增强热激活反转录转座子ONSEN的转录和跨代转座。我们提出，热诱导的ROS1转录抑制在植物物种中是保守的，它作为一种制动系统来限制转座元件的激活，从而保障基因组稳定性。
