Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation

Abstract

The ability of biotrophic fungi to metabolically adapt to the host environment is a critical factor in fungal diseases of crop plants. In this study, we analysed the transcriptome of maize tumours induced by Ustilago maydis to identify key features underlying metabolic shifts during disease. Among other metabolic changes, this analysis highlighted modifications during infection in the transcriptional regulation of carbohydrate allocation and starch metabolism. We confirmed the relevance of these changes by establishing that symptom development was altered in an id1 (indeterminate1) mutant that showed increased accumulation of sucrose as well as being defective in the vegetative to reproductive transition. We further established the relevance of specific metabolic functions related to carbohydrate allocation by assaying disease in su1 (sugary1) mutant plants with altered starch metabolism and in plants treated with glucose, sucrose and silver nitrate during infection. We propose that specific regulatory and metabolic changes influence the balance between susceptibility and resistance by altering carbon allocation to promote fungal growth or to influence plant defence. Taken together, these studies reveal key aspects of metabolism that are critical for biotrophic adaptation during the maize–U. maydis interaction.