Redox rhythm reinforces the circadian clock to gate immune response

The master immune regulator NPR1 of Arabidopsis is a sensor of the plant’s redox state and regulates transcription of core circadian clock genes even in the absence of pathogen challenge. In plants — and in many other eukaryotic organisms — the circadian clock ensures daily rhythmic fluctuations in biological processes not just by affecting gene transcription but also by modifying the organism's redox state. The molecular mechanism by which redox rhythms are linked to the circadian clock and the biological significance of redox–circadian interactions remain unclear. Xinnian Dong and colleagues identify an unexpected regulator of such redox rhythms in Arabidopsis. They find that the master immune regulator NPR1 senses a plant's redox state and regulates transcription of both the morning and evening core circadian-clock genes, independently of pathogenic infection. This network architecture helps plants to 'gate' their immune responses to the morning, thus minimizing the effect on growth, which occurs during the night. Recent studies have shown that in addition to the transcriptional circadian clock, many organisms, including Arabidopsis, have a circadian redox rhythm driven by the organism’s metabolic activities1,2,3. It has been hypothesized that the redox rhythm is linked to the circadian clock, but the mechanism and the biological significance of this link have only begun to be investigated4,5,6,7. Here we report that the master immune regulator NPR1 (non-expressor of pathogenesis-related gene 1) of Arabidopsis is a sensor of the plant’s redox state and regulates transcription of core circadian clock genes even in the absence of pathogen challenge. Surprisingly, acute perturbation in the redox status triggered by the immune signal salicylic acid does not compromise the circadian clock but rather leads to its reinforcement. Mathematical modelling and subsequent experiments show that NPR1 reinforces the circadian clock without changing the period by regulating both the morning and the evening clock genes. This balanced network architecture helps plants gate their immune responses towards the morning and minimize costs on growth at night. Our study demonstrates how a sensitive redox rhythm interacts with a robust circadian clock to ensure proper responsiveness to environmental stimuli without compromising fitness of the organism.