Singlet oxygen ((1)O2)-mediated signaling has been established in the conditional fluorescent (flu) mutant of Arabidopsis. In the dark, the flu mutant accumulates free protochlorophyllide (Pchlide), a photosensitizer that in the light generates (1)O2. The release of (1)O2 leads to growth inhibition of mature plants and bleaching of seedlings. These (1)O2-mediated responses depend on two plastid proteins, EXECUTER (EX) 1 and 2. An ex1/ex2/flu mutant accumulates in the dark Pchlide and upon illumination generates similar amounts of (1)O2 as flu, but (1)O2-mediated responses are abrogated in the triple mutant. The (1)O2- and EX-dependent signaling pathway operates also in wild type placed under light stress. However, it does not act alone as in flu, but interacts with other signaling pathways that modulate (1)O2-mediated responses. Depending on how severe the light stress is, (1)O2- and EX-dependent signaling may be superimposed by (1)O2-mediated signaling that does not depend on EX and is associated with photo-oxidative damage. Because of its high reactivity and short half-life, (1)O2 is unlikely to be a signal that is translocated across the chloroplast envelope, but is likely to interact with other plastid components close to its site of production and to generate more stable signaling molecules during this interaction. Depending on the site of (1)O2 production and the severity of stress, different signaling molecules may be expected that give rise to different (1)O2-mediated responses.