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

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Abstract

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 α,β-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 (EGSSG/2GSH) strongly correlated (R2 = 0.95) with decreasing Fv/Fm 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.

Graphical abstract

The involvement of reactive electrophile species (RES) in light stress responses of Chlamydomonas reinhardtii. Excess light increases the formation of singlet oxygen (1O2) from photosystem reaction centres in the chloroplast (green), which can induce lipid peroxidation of the thylakoid membrane lipids. Lipid peroxides decay to release RES (orange) that attack chloroplastic proteins, leading to protein carbonylation, but are also sensed by specific nuclear transcription factors (red), such as SOR1, whereby RES act as chloroplast-to-nucleus retrograde signals. Transcriptional alteration includes up-regulation of transcripts (white italics; black arrows) encoding mechanism that are involved in ROS and RES detoxification (GSTS1, FSD1, NTR3), including increasing glutathione (GSH1) and ascorbate (VTC2) contents. Other defence mechanisms include protecting proteins (HSP22, GRX2, GSTS1) and also mitigating excess light energy (LHCSR1, PSBS), thereby reducing light stress and RES formation. This pathway is superimposed over a false-coloured electron micrograph of an algal cell. The non-coloured region is the cytoplasm.

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