Endoplasmic reticulum‐mediated unfolded protein response is an integral part of singlet oxygen signalling in plants
Résumé
Singlet oxygen ($^1$O$_2$) is a by-product of photosynthesis that triggers a signalling pathway leading to stress acclimation or to cell death. By analyzing gene expressions in a $^1$O$_2^-$overproducing Arabidopsis mutant ($ch$1) under different light regimes, we show here that the $^1$O$_2$ signalling pathway involves the endoplasmic reticulum (ER)-mediated unfolded protein response (UPR). $ch$1 plants in low light exhibited a moderate activation of UPR genes, in particular $bZIP60$, and low concentrations of the UPR-inducer tunicamycin enhanced tolerance to photooxidative stress, together suggesting a role for UPR in plant acclimation to low $^1$O$_2$ levels. Exposure of ch1 to high light stress ultimately leading to cell death resulted in a marked upregulation of the two UPR branches ($bZIP60/IRE1$ and $bZIP28/bZIP17$). Accordingly, mutational suppression of $bZIP60$ and $bZIP28$ increased plant phototolerance, and a strong UPR activation by high tunicamycin concentrations promoted high light-induced cell death. Conversely, light acclimation of $ch$1 to $^1$O$_2$ stress put a limitation in the high light-induced expression of UPR genes, except for the gene encoding the BIP3 chaperone, which was selectively upregulated. $BIP3$ deletion enhanced Arabidopsis photosensitivity while plants treated with a chemical chaperone exhibited enhanced phototolerance. In conclusion, $^1$O$_2$ induces the ER-mediated UPR response that fulfils a dual role in high light stress: a moderate UPR, with selective induction of $BIP3$, is part of the acclimatory response to $^1$O$_2$, and a strong activation of the whole UPR is associated with cell death.