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

Abstract

SummarySinglet 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.

Singlet Oxygen in Plants: Generation, Detection, and Signaling Roles

“…The UPR is a stress reaction activated in response to the accumulation of aggregates of unfolded and misfolded proteins inside the ER lumen (ER stress) which aims at the restoration of normal ER functions but can elicit PCD if the adaptation was unsuccessful. The role of the URP in 1 O 2 -mediated PCD was further confirmed using ch1 mutants [109]. In ch1, expression of UPR genes was found to be constitutively enhanced compared to the situation in wild type plants, and increased further under high light conditions, eventually leading to cell death.…”

“…In ch1, expression of UPR genes was found to be constitutively enhanced compared to the situation in wild type plants, and increased further under high light conditions, eventually leading to cell death. Thus, a moderate UPR served as part of the acclimatory response of ch1 plants to 1 O 2 , and a strong activation of the whole UPR was associated with cell death [109]. Notably, some of UPR-related genes induced in ch1 were also induced in the flu mutant [109].…”

“…Thus, a moderate UPR served as part of the acclimatory response of ch1 plants to 1 O 2 , and a strong activation of the whole UPR was associated with cell death [109]. Notably, some of UPR-related genes induced in ch1 were also induced in the flu mutant [109]. It has been shown that URP in plants is regulated by SA [114].…”

“…Interestingly, 12-oxophytodienoic acid (OPDA), the precursor of JA, has an antagonistic effect on PCD initiated by JA in Arabidopsis suspension cell cultures [106]. 1 O 2 -induced PCD requires the synthesis of SA in both flu and ch1 mutants [88,109]. However, addition of the photosensitizer Rose Bengal to photosynthesizing Arabidopsis suspension cell cultures during moderate light stress elicited JA-and ethylene-dependent PCD while the EDS1 protein was not involved, suggesting that SA signaling was not required [106].…”

“…For instance, it was shown that during pathogen treatment, the red-chlorophyll-catabolite can move from chloroplasts to mitochondria and induce 1 O 2 -dependent PCD in mutants lacking the ACCELERATED CELL DEATH2 protein [105]. A recent study using the ceh1 mutant impaired in isoprenoid synthesis revealed another important player of 1 O 2 -mediated PCD, the endoplasmic reticulum (ER)-mediated unfolded protein response (UPR) [109]. The UPR is a stress reaction activated in response to the accumulation of aggregates of unfolded and misfolded proteins inside the ER lumen (ER stress) which aims at the restoration of normal ER functions but can elicit PCD if the adaptation was unsuccessful.…”