The adapt-to-nutrient NRPS-like secondary metabolite gene cluster facilitates Verticillium dahliae adaptation to different nutrient environments

Filamentous fungi produce a wide range of secondary metabolites to adapt to changing environments. RNA sequencing revealed that nine biosynthetic gene clusters (BGCs) of the phytopathogenic Verticillium dahliae react to different nutrient environments. The adapt-to-nutrient NRPS-like (ANN) cluster contributes to antibacterial activity and developmental processes important for the early biotrophic life cycle, but is dispensable for virulence on tomato (Solanum lycopersicum). Transcription of the core biosynthetic enzyme-encoding ANN3 is highly induced in nutrient-poor environment. ANN3 is transcriptionally controlled by global and in-cluster transcription factors. ANN3 is activated by early colonisation transcription factors Som1 and Vta2, but repressed by Mtf1, which governs late stages of disease progression. The in-cluster transcription factor Ann1, which represses ANN3, is less abundant in nutrient-poor environment or when V. dahliae encounters antagonists. Ann1 promotes resting structure formation but suppresses conidiation and antibacterial activity. Possible products of the ANN cluster were revealed by comparing metabolites extracted from ANN3 regulator mutants and from the bacterial-fungal interaction zone. Our findings revealed that V. dahliae perceives different nutrient environments and changes its survival strategy by differential expression of the ANN secondary metabolite gene cluster.