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The role of lipid signaling and metabolism in morphogenesis and pathogenesis of the fungal pathogen Ustilago maydis Klose, Jana

Abstract

The phytopathogenic fungus Ustilago maydis is obligately dependent on infection of maize to complete the sexual phase of its life cycle. Mating interactions between budding cells establish an infectious filamentous cell type that invades the host, induces tumors, and forms teliospores. The yeast-to-filamentous morphological transition is regulated by cAMP and MAPK signaling pathways known to control the pathogenic development in the host. The signals influencing this transition during infection have not yet been identified. In this study, we demonstrated that lipids triggered the dimorphic switch to promote a filamentous phenotype resembling the infectious filaments found in planta, which was dependent on cAMP and Ras/MAPK signaling. In addition, low levels of lipids (4nM) induced the response suggesting that they are acting as ligands to trigger the morphological change. Overall, lipids may represent one of the signals that promotes and maintains filamentation of the fungus in the host. To explore potential metabolic and signaling roles of lipids in morphogenesis and pathogenesis, we deleted genes encoding enzymes in the β-oxidation of fatty acids (mfe2, peroxisomal multifunctional enzyme; had1, mitochondrial 3-hydroxyacyl-CoA dehydrogenase) and a phospholipase A2 (lip2). Loss of mfe2 blocked extensive proliferation of fungal filaments in planta, delayed sporulation and reduced virulence. Loss of had1 resulted in attenuation of disease symptoms and impaired teliospore germination. These findings suggest that mitochondrial P-oxidation may be crucial during teliospore germination and initial stages of in planta fungal development, and that peroxisomal β-oxidation may be required during later stages of in planta development. In addition, Mfe2 and Had1 were specifically required for the filamentation induced by linoleic and myristic acid, respectively. Overall, lipids represent an important carbon source during biotrophic growth, and lipid utilization by U. maydis may influence additional aspects of infection (i.e., signal perception or host defense). Loss of lip2 resulted in more severe symptom development and more rapid teliospore maturation during infection. The Lip2 function might be important during fungus-host interactions to limit premature development of disease symptoms prior to sporulation. In summary, this work contributes to the emerging idea that lipid metabolism and signaling are important for biotrophic interactions between plants and fungal pathogens.

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