Acclimation of Chlamydomonas reinhardtii cells to low levels of singlet oxygen, produced either by photoreactive chemicals or high light treatment, induces a specific genetic response that strongly increases the tolerance of the algae to subsequent exposure to normally lethal singlet oxygen-producing conditions. The genetic response includes the increased expression of various oxidative stress response and detoxification genes, like the glutathione peroxidase homologous gene GPXH/GPX5 and the σ-class glutathione-S-transferase gene GSTS1. To identify components involved in the signal transduction and activation of the singlet oxygen-mediated response, a mutant selection was performed. This selection led to the isolation of the singlet oxygen resistant 1 (sor1) mutant, which is more tolerant to singlet oxygen-producing chemicals and shows a constitutively higher expression of GPXH and GSTS1. Map-based cloning revealed that the SOR1 gene encodes a basic leucine zipper transcription factor, which controls its own expression and the expression of a large number of oxidative stress response and detoxification genes. In the promoter region of many of these genes, a highly conserved 8-bp palindromic sequence element was found to be enriched. This element was essential for GSTS1 induction by increased levels of lipophilic reactive electrophile species (RES), suggesting that it functions as an electrophile response element (ERE). Furthermore, GSTS1 overexpression in sor1 requires the ERE, although it is unknown whether it occurs through direct binding of SOR1 to the ERE. RES can be formed after singlet oxygen-induced lipid peroxidation, indicating that RES-stimulated and SOR1-mediated responses of detoxification genes are part of the singlet oxygen-induced acclimation process in C. reinhardtii.