Redox rhythm reinforces the circadian clock to gate immune response

Nature. 2015 Jul 23;523(7561):472-6. doi: 10.1038/nature14449. Epub 2015 Jun 22.

Abstract

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 activities. 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 investigated. 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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / growth & development
  • Arabidopsis / immunology*
  • Arabidopsis / metabolism*
  • Arabidopsis / microbiology
  • Arabidopsis Proteins / biosynthesis
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Cell Nucleus / metabolism
  • Circadian Clocks / drug effects
  • Circadian Clocks / genetics
  • Circadian Clocks / physiology*
  • Circadian Rhythm / genetics
  • Circadian Rhythm / immunology
  • Circadian Rhythm / physiology
  • Darkness
  • Gene Expression Regulation, Plant / drug effects
  • Gene Expression Regulation, Plant / genetics
  • Genes, Plant / genetics
  • Oxidation-Reduction / drug effects
  • Plant Diseases / microbiology
  • Plant Immunity / genetics
  • Plant Immunity / immunology*
  • Pseudomonas syringae / physiology
  • Salicylic Acid / immunology
  • Salicylic Acid / metabolism
  • Salicylic Acid / pharmacology
  • Transcription Factors / biosynthesis
  • Transcription Factors / genetics
  • Transcription, Genetic / genetics

Substances

  • Arabidopsis Proteins
  • NPR1 protein, Arabidopsis
  • TOC1 protein, Arabidopsis
  • Transcription Factors
  • Salicylic Acid

Associated data

  • GEO/GSE61059