Pseudomonas putida KT2440 encodes three homologs of the LitR/CarH family (designated PplR1–PplR3), which is an adenosyl B12-dependent light-sensitive MerR family transcriptional regulator. Transcriptome analysis revealed the existence of a number of photo-inducible genes including pplR1, phrB (encoding DNA photolyase), ufaM (furan-containing fatty acid synthase), folE (GTP cyclohydrolase I), cryB (cryptochrome-like protein), and multiple genes without annotated/known function. Transcriptional analysis by quantitative RT-PCR with knockout mutants of pplR1–pplR3 showed that the triple knockout completely abolished the light-inducible transcription in P. putida, which indicates the occurrence of ternary regulation of PplR proteins. DNase I footprint assay showed that PplR1 protein specifically binds to the promoter regions of light-inducible genes, suggesting a consensus PplR1-binding direct repeat, 5′-T(G/A)TACAn12TGTA(C/T)A-3′. The disruption of B12 biosynthesis cluster did not affect the light-inducible transcription; however, disruption of ppSB1-LOV and ppSB2-LOV, encoding blue light photoreceptors adjacently located to pplR3 and pplR2, respectively, led to the complete loss of light-inducible transcription. Overall, the results suggest that the three PplRs and two PpSB-LOVs cooperatively regulate the light-inducible gene expression. The wide distribution of the pplR/ppSB-LOV cognate pair homologs in Pseudomonas spp. and related bacteria suggests that the response and adaptation to light is similarly regulated in the group of non-phototrophic bacteria. Importance LitR/CarH family is a new group of photosensor homologous to MerR-type transcriptional regulators. Proteins of this family are distributed to various non-phototrophic bacteria and grouped into at least five (I-V) classes. Pseudomonas putida retaining three class II LitR proteins exhibited genome-wide response to light. All three paralogs were functional and mediated photo-dependent activation of promoters directing the transcription of light-induced genes or operons. Two LOV (light-oxygen-voltage)-domain proteins adjacently encoded to two litR genes were also essential for the photo-dependent transcriptional control. Despite the difference in light-sensing mechanism, the DNA binding consensus of class II LitR [T(G/A)TA(C/T)A] was the same as that of class I. This is the first study showing the actual involvement of class II LitR in light-induced transcription.