The role of salicylic acid on glutathione metabolism under endoplasmic reticulum stress in tomato

Abstract

The endoplasmic reticulum (ER) stress and the unfolded protein response (UPR) are highly dependent on phytohormones such as salicylic acid (SA). In this study, the effect of SA supplementation and the lack of endogenous SA on glutathione metabolism were investigated under ER stress in wild-type (WT) and transgenic SA-deficient NahG tomato (Solanum lycopersicum L.) plants. The expression of the UPR marker gene SlBiP was dependent on SA levels and remained lower in NahG plants. Exogenous application of the chemical chaperone 4-phenylbutyrate (PBA) also reduced tunicamycin (Tm)-induced SlBiP transcript accumulation. At the same time, Tm-induced superoxide and hydrogen peroxide production were independent of SA, whereas the accumulation of reduced form of glutathione (GSH) and the oxidised glutathione (GSSG) was regulated by SA. Tm increased the activity of glutathione reductase (GR; EC 1.6.4.2) independently of SA, but the activities of dehydroascorbate reductase (DHAR; EC 1.8.5.1) and glutathione S-transferases (GSTs; EC 2.5.1.18) were increased by Tm in a SA-dependent manner. SlGR2, SlGGT and SlGSTT2 expression was activated in a SA-dependent way upon Tm. Although expression of SlGSH1, SlGSTF2, SlGSTU5 and SlGTT3 did not change upon Tm treatment in leaves, SlGR1 and SlDHAR2 transcription decreased. PBA significantly increased the expression of SlGR1, SlGR2, SlGSTT2, and SlGSTT3, which contributed to the amelioration of Tm-induced ER stress based on the changes in lipid peroxidation and cell viability. Malondialdehyde accumulation and electrolyte leakage were significantly higher in WT as compared to NahG tomato leaves under ER stress, further confirming the key role of SA in this process.