Light-sensing via hydrogen peroxide and a peroxiredoxin

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.

The Two Cryptochrome/Photolyase Family Proteins Fulfill Distinct Roles in DNA Photorepair and Regulation of Conidiation in the Gray Mold Fungus Botrytis cinerea

“…Furthermore, photoperception could be related to photoreceptor-independent light-sensing mechanisms such as those described recently for Saccharomyces cerevisiae. Here, a peroxisomal oxidase generates H 2 O 2 in a light-dependent manner, and the H 2 O 2 is sensed by a peroxiredoxin to induce signaling (54). Whereas the addition of exogenous H 2 O 2 bypasses the requirement for the peroxisomal oxidase in yeast (54), it is not sufficient to induce conidiation in B. cinerea (J. Schumacher, unpublished data).…”

Hydrogen peroxide metabolism and functions in plants

“…ROS (H 2 O 2 ) production from cryptochrome, a blue light photoreceptor, occurs in Arabidopsis and Drosophila (Consentino et al ., ; Arthaut et al ., ). Other flavin‐containing enzymes could also generate O 2 ·− and then H 2 O 2 in the light, and it has been shown that a yeast mutant in peroxisomal acyl‐CoA oxidase is impaired in light‐induced H 2 O 2 production and downstream signalling (Bodvard et al ., ). As yeast lacks conventional photoreceptors, another flavin‐dependent protein must provide light–dark or circadian cues.…”

“…Given the contradictory nature of the evidence so far, it will be important to determine whether peroxisomes are always net sinks or whether they can also be sources. Interestingly, strong evidence for a specific signalling role for peroxisome‐sourced H 2 O 2 has been demonstrated in yeast (Bodvard et al ., ). Other features of peroxisome activity that will impinge on this question are the proliferation and increased mobility under oxidative stresses and the formation of peroxule extensions (Rodríguez‐Serrano et al ., ).…”

Oxidative stress tolerance of a spore clone isolated from Shirakami kodama yeast depends on altered regulation of Msn2 leading to enhanced expression of ROS-degrading enzymes

“…H 2 O 2 can act as a second message and is then transduced by peroxiredoxin, which relays the signal to thioredoxin (Trx). Oxidized thioredoxins inhibit PKA-dependent phosphorylation, allowing Msn2 and Msn4 to concentrate in the nucleus (Bodvard et al, 2017). Kinases Rim15 and Yak1 can positively regulate Msn2/4 dependent transcription, for example of starvation-specific genes (Zhang et al, 2013).…”