Formation of the photosynthetic apparatus in Rhodobacter is regulated by oxygen tension and light intensity. Here we show that in anaerobically grown Rhodobacter cells a light-dependent increase in expression of the puc and puf operons encoding structural proteins of the photosynthetic complexes requires an active photosynthetic electron transport. The redox-sensitive CrtJ/PpsR repressor of photosynthesis genes, which was suggested to mediate electron transport-dependent signals, is not involved in this light-dependent signal chain. Our data reveal that the signal initiated in the photosynthetic reaction centre is transmitted via components of the electron transport chain and the PrrB/PrrA two-component system in Rhodobacter sphaeroides. Under blue light illumination in the absence of oxygen this signal leads to activation of photosynthesis genes and interferes with a blue-light repression mediated by the AppA photoreceptor and the PpsR transcriptional repressor in R. sphaeroides. Thus, light either sensed by a photoreceptor or initiating photosynthetic electron transport has opposite effects on the transcription of photosynthesis genes. Both signalling pathways involve redox-dependent steps that finally determine the effect of light on gene expression.