Blue light-dependent development of the filamentous fungus Aspergillus nidulans

Abstract

Numerous studies have revealed that fungal development and the production of secondary metabolites are linked although the molecular mechanisms are yet unknown. Light seems to be one of the environmental triggers for the coordination of these processes. Here, the light-controlled synchronization of the formation of sexual fruitbodies (cleistothecia) and secondary metabolism was analysed in the filamentous model fungus Aspergillus nidulans. The light response of the fungus was addressed by analyzing a cryptochrome-like gene product as putative blue light receptor. A. nidulans carries a single gene in its genome, termed cryA, with the capacity to encode a cryptochrome/photolyase-like protein. We aimed at the characterization of cryA and its product as a first fungal cryptochrome. Detailed interpretation of experimental results and findings revealed that the A. nidulans CryA is a unique protein among the cryptochrome/photolyase-like protein family because it is a dual function protein which regulates gene expression in A. nidulans: it repairs UV-induced DNA damage both in a UV repair defective E.coli and in A. nidulans. Expression experiments revealed that it regulates a novel transcriptional feedback loop including the so-called light-dependent velvet regulatory protein. Expression of the veA gene is affected by CryA activity. The A. nidulans velvet A gene, veA, is an essential component of the light-dependent sexual development regulation whose function is inhibited in day light (red light) and actived in the absence of light (darkness). veA represses asexual development and promotes sexual fruit body formation in A. nidulans. Here, an orthologue of velvet in the heterothallic fungus Neurospora crassa, and showed that the N.crassa velvet, ve-1, is conserved structurally and functionally. It also regulates fungal development resulting in stunted hyphal growth and increased asexual conidiation of mutant strains. In addition to its role in sexual development in A. nidulans, veA is also involved in the regulation of secondary metabolism, since deletion of veA results in a complete loss of cleistothecia formation and the loss of sterigmatocystin production as well as downregulation of the expression of genes responsible for penicillin biosynthesis. The molecular mechanism of this connection between light control and secondary metabolism is yet unknown and has been addressed in this work, too. For this purpose, interaction partners of VeA were identified using a generic Tandem Affinity Purification (TAP) tag approach. It turned out that VeA is a part of a trimeric protein complex constituted by VelB, VeA and the putative LaeA methyl transferase, a master regulator of secondary metabolism. This newly defined velvet complex appears to regulate both light-dependent sexual development and secondary metabolism in A. nidulans.