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.

How to make a tumour: cell type specific dissection ofUstilago maydis‐induced tumour development in maize leaves

“…Nevertheless, this result is consistent with previous studies that described an increase in starch content of chloroplasts inside infected areas (Snetselaar & Mims, ). However, several previous studies on starch content in U. maydis ‐infected tissue reported diverse results (Doehlemann et al ., ; Horst et al ., ; Kretschmer et al ., 2016b). Besides an influence of different sampling conditions and varying types of tissue, this also indicates that the U. maydis ‐induced starch accumulation is a very local effect, which is restricted to the tumorous tissue.…”

Chloroplast‐associated metabolic functions influence the susceptibility of maize to Ustilago maydis

“…() revealed that functions for photosynthesis, such as CO 2 fixation, chlorophyll biosynthesis or photosystem‐related proteins of the chloroplast, were down‐regulated during tumour formation (Table , see Fig. S1 and Text S1, Supporting Information; Kretschmer et al ., ). The observed negative impact on the expression of chloroplast functions is interesting because of the chlorosis and chlorophyll changes that occur in tumours at later stages of disease, as is macroscopically evident from their white appearance (Horst et al ., ; Fig.…”

“…This approach allows the scoring of increased and decreased symptoms of the infected plants. The infections were scored after 14 days, as described previously (Kretschmer et al ., ). For why1‐2 , the number of plants available for the study was somewhat limited.…”

“…A hallmark of tumour formation is chlorosis, and previous transcriptome and metabolic studies have revealed that infection by U. maydis impairs C 4 photosynthesis (Doehlemann et al ., ; Horst et al ., ). In addition, tumour induction results in increased transcript levels for plant defence functions and enzymes for amino acid biosynthesis, secondary metabolism and the tricarboxylic acid (TCA) cycle, among other functions (Doehlemann et al ., ; Horst et al ., ; Kretschmer et al ., ). In general, infection results in the establishment of tumour tissue as a sink for amino acids and carbohydrates with particular changes to sucrose biosynthesis and transport (Horst et al ., ).…”

“…In this study, we made use of our RNA‐sequencing (RNA‐Seq) data for tumour tissue to predict key metabolic changes during disease with the goal of understanding which differences favour the pathogen versus the host (Kretschmer et al ., ). We found that U. maydis probably impacts chloroplast function during disease and identified key associated activities.…”