Control of DNA demethylation by superoxide anion in plant stem cells

Abstract Superoxide anion is thought to be a harmful natural byproduct with strong oxidizing ability in all living organisms and was recently found to accumulate in plant meristems to maintain stem cells in the shoot and undifferentiated meristematic cells in the root. Here, we show that the DNA demethylases Repressor of Silencing 1 (ROS1) is one of the direct targets of superoxide in stem cells. The Fe-S clusters in ROS1 are oxidized by superoxide to activate its DNA glycosylase/lyase activity. We demonstrate that superoxide extensively participates in the establishment of active DNA demethylation in the Arabidopsis genome and that ARABIDOPSIS RESPONSE REGULATOR 12 (ARR12) acts downstream of ROS1-mediated superoxide signaling to maintain stem cell fate. Our results provide a mechanistic framework for superoxide control of the stem cell niche and demonstrate how redox and DNA demethylation interact to define stem cell fate in plants.