The adenylyl cyclase plays a regulatory role in the morphogenetic switch from vegetative to pathogenic lifestyle of Fusarium graminearum on wheat

• Published in: PloS one Vol. 9; no. 3; p. e91135
• Main Authors: Bormann, Jörg, Boenisch, Marike Johanne, Brückner, Elena, Firat, Demet, Schäfer, Wilhelm
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 06-03-2014; Public Library of Science (PLoS)
• Subjects: Adenosine monophosphate; Adenosine triphosphate; Adenylyl Cyclases - metabolism; Agar; Anastomosis; Appressoria; ATP; Barley; Biological Assay; Biology; Biosynthesis; Blight; Cellular manufacture; Cellular structure; Clonal deletion; Conidia; Corn; Cushions; Cyclic adenosine monophosphate; Cyclic AMP; Cyclic AMP - metabolism; Cytosol - metabolism; Deletion mutant; Deoxynivalenol; Electron microscopy; Enzymes; Epidermis; Fluorescence; Fluorescence microscopy; Fungi; Fusarium; Fusarium - enzymology; Fusarium - growth & development; Fusarium - pathogenicity; Fusarium graminearum; Gene Deletion; Health aspects; Host Specificity; Hyphae; Infections; Kinases; Lesions; Life cycle engineering; Life cycles; Magnaporthe grisea; Magnaporthe oryzae; Membrane proteins; Morphogenesis; Mutation - genetics; Oryza; Pathogenicity; Pathogens; Perithecia; Plant Diseases - microbiology; Protein binding; Proteins; Reproduction (biology); Rhizoctonia solani; Scanning electron microscopy; Sexual reproduction; Signal Transduction; Signaling; Spores, Fungal - growth & development; Sporulation; Trichothecenes - biosynthesis; Triticum - microbiology; Ustilago maydis; Wheat
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0091135

Cyclic 3',5'-adenosine monophosphate (cAMP) is a nucleotide derived from adenosine triphosphate that acts as a second messenger throughout all kingdoms. Intracellular cAMP levels are synthesized by a membrane-bound protein, the adenylyl cyclase. In order to analyze the function of this gene and the importance of cAMP in the life cycle of the cereal pathogen Fusarium graminearum, the adenylyl cyclase gene (FGSG_01234) was deleted by gene replacement (ΔFgac1). The ΔFgac1 mutant displayed a drastically reduced growth on agar medium which could be rescued by a cAMP analogon. Furthermore, the ΔFgac1 mutant was unable to produce perithecia on detached wheat nodes. However, artificial conditions like carrot agar allowed perithecia development. Pathogenicity towards wheat was drastically reduced in ΔFgac1 compared to the wild type. Point-inoculated spikelets showed only small lesions but no typical head blight disease symptoms. Fluorescence microscopy using dsRed-expressing strains revealed that the ΔFgac1 strain was unable to develop any complex infection structures like lobate appressoria and infection cushions. Instead, hyphal anastomosis occurs frequently. Scanning electron microscopy demonstrated the lack of fungal penetration. Hence, the formation of compound appressoria seems to be essential for infection of wheat. Hyphae on flower leaves produced huge amounts of new conidia, thereby circumventing the infection cycle. This abundant sporulation on wheat epidermis was not observed in wild type. Intriguingly, the Fgac1 deletion mutant was able to infect maize cobs as wild type, indicating that cAMP signaling is not important for maize infection. The ΔFgac1 mutant was unable to produce the mycotoxin deoxynivalenol both in vitro and during wheat infection. In this study, we show that cAMP signaling controls important cellular processes such as development of infection structures, pathogenicity, secondary metabolite production and sexual reproduction. For the first time, we show that cAMP regulates the switch from vegetative to pathogenic lifestyle of F. graminearum on wheat.