GPCR-mediated glucose sensing system regulates light-dependent fungal development and mycotoxin production

• Published in: PLoS genetics 2019-10, Vol.15 (10), p.e1008419-e1008419
• Main Authors: Dos Reis, Thaila Fernanda, Mellado, Laura, Lohmar, Jessica M, Silva, Lilian Pereira, Zhou, Jing-Jiang, Calvo, Ana M, Goldman, Gustavo H, Brown, Neil A
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - radiation effects; Aspergillus nidulans - physiology; Authorship; Bioengineering; Biology and Life Sciences; Carbon; Carbon - metabolism; Chemoreception; Cyclic adenosine monophosphate; Cyclic AMP; Epistasis; Funding; Fungal Proteins - metabolism; Fungi; G protein-coupled receptors; Gene Expression Profiling; Gene Expression Regulation, Fungal - radiation effects; Genetic engineering; Genomes; Genomics; Germination; Glucose; Glucose - metabolism; Kinases; Laboratories; Ligands; Light; Metabolism; Metabolites; Microorganisms; Morphogenesis; Mutation; Novels; Nutrients; Phosphorylation; Physical Sciences; Physiological aspects; Protein kinase A; Proteins; Receptors, G-Protein-Coupled - metabolism; Research and Analysis Methods; Sexual development; Spores, Fungal - growth & development; Spores, Fungal - radiation effects; Sterigmatocystin; Sterigmatocystin - biosynthesis; Supervision; Transcription factors
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1008419

Microorganisms sense environmental fluctuations in nutrients and light, coordinating their growth and development accordingly. Despite their critical roles in fungi, only a few G-protein coupled receptors (GPCRs) have been characterized. The Aspergillus nidulans genome encodes 86 putative GPCRs. Here, we characterise a carbon starvation-induced GPCR-mediated glucose sensing mechanism in A. nidulans. This includes two class V (gprH and gprI) and one class VII (gprM) GPCRs, which in response to glucose promote cAMP signalling, germination and hyphal growth, while negatively regulating sexual development in a light-dependent manner. We demonstrate that GprH regulates sexual development via influencing VeA activity, a key light-dependent regulator of fungal morphogenesis and secondary metabolism. We show that GprH and GprM are light-independent negative regulators of sterigmatocystin biosynthesis. Additionally, we reveal the epistatic interactions between the three GPCRs in regulating sexual development and sterigmatocystin production. In conclusion, GprH, GprM and GprI constitute a novel carbon starvation-induced glucose sensing mechanism that functions upstream of cAMP-PKA signalling to regulate fungal development and mycotoxin production.