Photosynthetic bacteria regulate photosystem synthesis in response to alterations in oxygen tension and light intensity. In this study we show that the PpsR repressor from Rhodobacter sphaeroides binds to DNA in a redox-dependent manner through the formation/breakage of an intramolecular disulfide bond. We also demonstrate that PpsR is antagonized by the flavin-containing antirepressor, AppA, that is capable of breaking the disulfide bond in oxidized PpsR as well as forming a stable AppA-PpsR(2) antirepressor-repressor complex. Blue light excitation of AppA induces a photocycle that is characterized by a long-lived red-shifted absorbance of the flavin. Light-excited AppA was found to be incapable of forming the AppA-PpsR(2) antirepressor complex. These results establish AppA as a transcription factor that controls both redox and blue light repression of photosystem gene expression by mediating DNA binding activity of PpsR.