Distress and eustress of reactive electrophiles and relevance to light stress acclimation via stimulation of thiol/disulphide-based redox defences

Photosynthetic organisms suffering from light stress have to cope with an increased formation of reactive short-chain aldehydes. Singlet oxygen generated from highly-charged reaction centres can peroxidise the poly-unsaturated fatty acid (PUFA)-rich thylakoid membranes they are embedded in. Lipid peroxides decay to release alpha,beta-unsaturated aldehydes that are reactive electrophile species (RES). Acrolein is one of the most abundant and reactive RES produced in chloroplasts. Here, in the model chlorophyte alga Chlamydomonas reinhardtii, a clear concentration-dependent distress induced by acrolein intoxication was observed in conjunction with depletion of the glutathione pool. The glutathione redox state (E-GssG/2GsH) strongly correlated (R-2 = 0.95) with decreasing F-v/F-m values of chlorophyll fluorescence. However, treatment of C. reinhardtii with sub-toxic acrolein concentrations increased glutathione concentrations and raised the protein levels of a glutathione-S-transferase (GSTS1), mimicking the response to excess light, indicating that at lower concentrations, acrolein may contribute to high light acclimation, which could be interpreted as eustress. Furthermore, similar patterns of chloroplastic protein carbonylation occurred under light stress and in response to exogenous acrolein. Priming cells by low doses of acrolein increased the alga's resistance to singlet oxygen. A RNA seq. analysis showed a large overlap in gene regulation under singlet oxygen and acrolein stresses. Particularly enriched were transcripts of enzymes involved in thiol/disulphide exchanges. Some of the genes are regulated by the SOR1 transcription factor, but acrolein treatment still induced an increase in glutathione contents and enhanced singlet oxygen tolerance of the sor1 mutant. The results support a role for RES in chloroplast-to-nucleus retrograde signalling during high light acclimation, with involvement of SOR1 and other pathways.