H2O2 repurposes the plant oxygen-sensing machinery to control the transcriptional response to oxidative stress

Abstract

Plants sense reduced oxygen availability (hypoxia) through Plant Cysteine Oxidases (PCOs). Reduced PCO activity in hypoxia, as seen during submergence, stabilises Group VII Ethylene Response Factors (ERFVIIs), master regulators of adaptive metabolic and anatomic responses. Equally important is timely arrest of these responses upon reoxygenation, assumed to occur through ERFVII degradation. Reoxygenation involves reactive oxygen species (ROS) production. Here, we report that instead of degradation, reoxygenation results in ERFVII nuclear stabilisation, an effect mimicked by direct H2O2 treatment. Interestingly, typical hypoxia marker genes are repressed while genes involved in ROS homeostasis and oxidative stress protection are upregulated. Using in planta, heterologous and biochemical assays, we reveal that ROS-related ERFVII stabilisation is caused by PCO inactivation. Stabilised ERFVIIs are retained at hypoxia-responsive promoters but become repressors. Our findings suggest that by responding to both oxygen and ROS, PCOs coordinate ERFVII stability to regulate timely responses to damaging fluctuations in oxygen availability.