The virulence hub of Ustilago maydis: contributions of mitochondria and mitochondrial metabolism to filamentation, mating, melanin and extracellular matrix formation

Matthias Kretschmer 1 Scott Lambie 1 Daniel Croll 2 James Kronstad 1
1Michael Smith Laboratories, University of British Columbia, Vancouver, Canada
2Laboratory of Evolutionary Genetics, University of Neuch√Ętel, Neuch√Ętel, Switzerland

The ability of pathogens to exploit host nutrients to support growth is a key aspect of infectious disease. The biotrophic fungal pathogen Ustilago maydis, the cause of common smut on corn, forms an infectious filamentous cell type that induces tumor formation in the host. Massive proliferation and the formation of spores fulfil its lifecycle. Nutritional requirements that support hyphal growth and lead to sporulation in planta are poorly understood. We previously showed that a wide range of fatty acids, a non-preferred carbon source, induced filamentation for haploid cells in vitro. Here we show that another non-preferred carbon source, acetate, does not support filamentation upon mating, and inhibits filamentation induced by oleic acid. We used RNAseq to identify transcriptional changes of U. maydis on non-prefered carbon sources such as acetate and oleic acid, and compared expression patterns to those for the preferred carbon source glucose and in planta growth. Transcriptional changes indicated that acetate negatively influenced cellular stress resistance, induced reactive oxygen formation, interfered with mitochondrial functions and inhibited mating even under inducing conditions. Specific phenotypic assays confirmed the transcriptional conclusions. Furthermore, acetate was able to reduce the virulence of U. maydis. Mitochondrial functions and metabolism such as the tricarboxylic acid (TCA) cycle and the electron transport chain (ETC) are involved in growth on non-preferred carbon sources, filamentation and mating in U. maydis. Furthermore, TCA cycle intermediates, but not glyoxylate, in combination with glucose, triggered phenotypes normally limited to sporulation in planta, including the formation of an extracellular matrix, melanin production and morphological changes. Our results suggest a complex interplay of different preferred and non-preferred carbon sources for a biotrophic pathogen to fulfil its life cycle.