Circadian redox rhythm gates immune-induced cell death distinctly from the genetic clock

Abstract

Organisms use circadian clocks to synchronize physiological processes to anticipate the Earths day-night cycles and regulate responses to environmental stresses to gain competitive advantage1. While divergent genetic clocks have been studied extensively in bacteria, fungi, plants, and animals, a conserved circadian redox rhythm has only recently been reported and hypothesized to be a more ancient clock2, 3. However, it is controversial whether the redox rhythm serves as an independent clock and controls specific biological processes4. Here, we uncovered the coexistence of redox and genetic rhythms with distinct period lengths and transcriptional targets through concurrent metabolic and transcriptional time-course measurements in an Arabidopsis long-period clock mutant5. Analysis of the target genes indicated regulation of the immune-induced programmed cell death (PCD) by the redox rhythm. Moreover, this time-of-day-sensitive PCD was eliminated by redox perturbation and by blocking the signalling pathway of the plant defence hormones jasmonic acid/ethylene, while remaining intact in a genetic-clock-impaired line. We demonstrate that compared to robust genetic clocks, the more sensitive circadian redox rhythm serves as a signalling hub in regulating incidental energy-intensive processes, such as immune-induced PCD6, to provide organisms a flexible strategy to prevent metabolic overload caused by stress, a unique role for the redox oscillator.