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

Singlet oxygen (O-1(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 (ch1) under different light regimes, we show here that the(1)O(2)signalling pathway involves the endoplasmic reticulum (ER)-mediated unfolded protein response (UPR).ch1plants in low light exhibited a moderate activation of UPR genes, in particularbZIP60, 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 ofch1to 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 ofbZIP60andbZIP28increased plant phototolerance, and a strong UPR activation by high tunicamycin concentrations promoted high light-induced cell death. Conversely, light acclimation ofch1to(1)O(2)stress put a limitation in the high light-induced expression of UPR genes, except for the gene encoding theBIP3chaperone, which was selectively upregulated.BIP3deletion 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 ofBIP3, is part of the acclimatory response to(1)O(2), and a strong activation of the whole UPR is associated with cell death.