A global analysis of photoreceptor-mediated transcriptional changes reveals the intricate relationship between central metabolism and DNA repair

Light provides critical information for the behavior and development of basically all organisms. Filamentous fungi sense blue light through a unique transcription factor complex that activates its targets in a light-dependent manner. In Trichoderma atroviride, the Blr-1 and Blr-2 proteins constitute this complex, which triggers the light-dependent formation of asexual reproduction structures (conidia). Using transcriptomics, we identified the genes regulated by the photoreceptors Blr-1, Blr-2, Cry-1, Cry-DASH, and Envoy. The evaluation of the transcriptional response to blue light of the Δblr-1 and Δblr-2 mutants showed that the BLR proteins have common targets, which indicates that these proteins act as a complex in gene regulation. Nevertheless, the severe alteration in the transcriptional profile of the Δblr-2 strain indicates that Blr-2 provides target specificity to the protein complex, while Blr-1 central role is as a transcriptional activator. The Δenv-1 mutant phenotypic characterization showed that Envoy functions as a growth and conidiation checkpoint, preventing excessive light responses. Similarly, we observed that Cry-1 and Cry-DASH contribute to the typical light-induced conidiation response. In the env-1 mutant, we observed, at the transcriptomic level, a general induction of DNA metabolic processes and strong repression of central metabolism. An analysis of the expression level of DNA repair genes showed that they increase their expression in the absence of Envoy. Photoreactivation experiments showed that Δenv-1 had increased DNA repair capacity, which is consistent with the transcriptomic data. Our results indicate that light perception in T. atroviride is far more complex than originally thought.