Alterations in gene expression and secondary metabolite production during development of Aspergillus nidulans

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Many studies describing development and secondary metabolism of the filamentous fungus Aspergillus nidulans contributed to a better understanding of fungal secondary metabolism regulation at the molecular level. However, a comprehensive picture of the regulation remained to be shown. Therefore, in this work we undertake a global transcriptomic and metabolomic overview, which describes the light-dependent developmental responses of this soil-borne fungus. Light favours the development of asexual spores and inhibits the formation of sexual fruiting bodies (cleistothecia), which are preferentially formed in the absence of light. Overall 2.014 genes, which correspond to 20 % of the genome, are differentially expressed and influenced during different developmental stages in the light and in the dark. Light controls development by inducing gene expression significantly during 24-48 hours of development. Targeted repression of light sensing complexes in early sexual development might delay differentiation and gene expression. Increased numbers of delayed genes during sexual differentiation reveal temporal consistency with the secondarily induced, delayed conidiation at sexual development. Interestingly, transcriptomics of vegetative growth and early sexual development exhibit similar profiles, which is consistent with highly similar growth phenotypes. A characteristic feature during the late phase of asexual spore formation of light-induced asexual development is the expression of stress response genes, which might provide resistance to various abiotic stress conditions, including UV irradiation and related oxidative stress compounds for the air-borne conidia. Fungal development depends on psi (precocious sexual inducer) factors, which are oxylipin hormones related to prostaglandins. PsiC1 (5,8-DiHOE) appears specifically in darkness during early sexual development. During the sexual cycle A. nidulans initiates the expression of many genes required for cell wall degradation, including genes for plant and bacterial cell wall and polysaccharides hydrolysis, which probably mobilize the energy and building blocks for the completion of sexual fruiting bodies during nutrient limitations. During the late sexual stage, protective secondary metabolites are present, which might be crucial to protect the fruiting bodies against fungivors and therefore, helping ascospores to germinate in the presence of a decreased number of competitors. The emericellamide C metabolite is secreted before the cleistothecia maturation and completion of sexual development. Many downregulated amino acid biosynthetic genes and cellular amino acids levels at late sexual development indicate a period of dormancy where translation stops due to lacking amino acids. Fungus initiates programmed cell death at late sexual development by inducing apoptotic gene expression, which corresponds to an aging process. Our results revealed that during light-dependent fungal development, a significant proportion of the genome (20 %) is affected by the light signal, which leads to various responses, including production of secondary metabolites and other adaptive responses, collectively contributing the fungus to adapt and survive through the current environmental conditions.