Endoplasmic reticulum-mediated unfolded protein response is an integral part of singlet oxygen signalling in plants

Singlet oxygen (1O2) 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 1O2-overproducing Arabidopsis mutant (ch1) under different light regimes, we show here that the 1O2 signalling pathway involves the endoplasmic reticulum (ER)-mediated unfolded protein response (UPR). ch1 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 1O2 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 ch1 to 1O2 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, 1O2 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 1O2, and a strong activation of the whole UPR is associated with cell death.