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

Summary 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 ( 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). 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 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 ch1 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.