The chloroplast psbD-psbC loci, which encode the D2 and CP43 subunits of the photosystem II reaction center, respectively, are regulated by a blue light-responsive promoter (BLRP). It has recently been shown in barley seedlings that activation of psbD-psbC transcription by blue light involves inhibition of a protein kinase that represses the BLRP in the dark. To elucidate further the photosensory pathways regulating the psbD BLRP, the effects of three nuclear mutations on the expression of the BLRP in chloroplasts of Arabidopsis thaliana were examined. The mutants used included the det1-1 and det1-6 alleles for the nuclear protein DET1, involved in repressing photomorphogenesis, and the cry1 gene for the blue light photoreceptor, cryptochrome (CRY1), involved in hypocotyl elongation. The BLRP was not significantly expressed in cotyledons of light-grown wild-type seedlings, unlike the light-responsive expression of the chloroplast, psbA and rbcL, and nuclear, Lhcb and Chs, genes. Analysis of the mutants revealed that DET1 represses transcription from the BLRP in a developmental and tissue-specific manner, which is unique from the effects that DET1 has on other light-regulated promoters. In addition, the cry1 mutation did not reduce the expression of the BLRP in response to blue light. This suggests that the BLRP is regulated by a different photosensory system relative to CRY1. A model is proposed involving blue light, DET1 and phytochrome in regulating transcription from the psbD BLRP.