BackgroundAdaptation to complex, rapidly changing environments is crucial for evolutionary success of fungi. The heterotrimeric G-protein pathway belongs to the most important signaling cascades applied for this task. InTrichoderma reesei,enzyme production, growth and secondary metabolism are among the physiological traits influenced by the G-protein pathway in a light dependent manner.ResultsHere, we investigated the function of the SNX/H-type regulator of G-protein signaling (RGS) protein RGS4 ofT. reesei. We show that RGS4 is involved in regulation of cellulase production, growth, asexual development and oxidative stress response in darkness as well as in osmotic stress response in the presence of sodium chloride, particularly in light. Transcriptome analysis revealed regulation of several ribosomal genes, six genes mutated in RutC30 as well as several genes encoding transcription factors and transporters. Importantly, RGS4 positively regulates the siderophore cluster responsible for fusarinine C biosynthesis in light. The respective deletion mutant shows altered growth on nutrient sources related to siderophore production such as ornithine or proline in a BIOLOG phenotype microarray assay. Additionally, growth on storage carbohydrates as well as several intermediates of the D-galactose and D-arabinose catabolic pathway is decreased, predominantly in light.ConclusionsWe conclude that RGS4 mainly operates in light and targets plant cell wall degradation, siderophore production and storage compound metabolism inT. reesei.Supplementary InformationThe online version contains supplementary material available at 10.1186/s12864-023-09467-2.