Abstract
Yeast lacks dedicated photoreceptors; however, blue light still causes pronounced oscillations of the transcription factor Msn2 into and out of the nucleus. Here we show that this poorly understood phenomenon is initiated by a peroxisomal oxidase, which converts light into a hydrogen peroxide (H2O2) signal that is sensed by the peroxiredoxin Tsa1 and transduced to thioredoxin, to counteract PKA-dependent Msn2 phosphorylation. Upon H2O2, the nuclear retention of PKA catalytic subunits, which contributes to delayed Msn2 nuclear concentration, is antagonized in a Tsa1-dependent manner. Conversely, peroxiredoxin hyperoxidation interrupts the H2O2 signal and drives Msn2 oscillations by superimposing on PKA feedback regulation. Our data identify a mechanism by which light could be sensed in all cells lacking dedicated photoreceptors. In particular, the use of H2O2 as a second messenger in signalling is common to Msn2 oscillations and to light-induced entrainment of circadian rhythms and suggests conserved roles for peroxiredoxins in endogenous rhythms.
Highlights
Yeast lacks dedicated photoreceptors; blue light still causes pronounced oscillations of the transcription factor Msn[2] into and out of the nucleus
We show that in S. cerevisiae a conserved peroxisomal oxidase converts the light impulse into a H2O2 signal that is sensed by the peroxiredoxin Tsa[1] and transduced to thioredoxin to inhibit protein kinase A (PKA) activity
We propose that peroxiredoxin-mediated H2O2 signalling establishes rhythmic Msn[2] nuclear accumulation by superimposing on PKA feedback regulation
Summary
Yeast lacks dedicated photoreceptors; blue light still causes pronounced oscillations of the transcription factor Msn[2] into and out of the nucleus. We show that this poorly understood phenomenon is initiated by a peroxisomal oxidase, which converts light into a hydrogen peroxide (H2O2) signal that is sensed by the peroxiredoxin Tsa[1] and transduced to thioredoxin, to counteract PKA-dependent Msn[2] phosphorylation. The use of H2O2 as a second messenger in signalling is common to Msn[2] oscillations and to light-induced entrainment of circadian rhythms and suggests conserved roles for peroxiredoxins in endogenous rhythms. We show that in S. cerevisiae a conserved peroxisomal oxidase converts the light impulse into a H2O2 signal that is sensed by the peroxiredoxin Tsa[1] and transduced to thioredoxin to inhibit PKA activity. We report that the Tsa1-mediated signal counteracts the nuclear retention of the two most highly expressed of the PKA catalytic subunits, thereby antagonizing a process that contributes to delayed Msn[2] nuclear localization in response to H2O2
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