Abstract
The basidiomycete Ustilago maydis is the causal agent of corn smut disease and induces tumor formation during biotrophic growth in its host maize (Zea mays). We have conducted a combined metabolome and transcriptome survey of infected leaves between 1 d post infection (dpi) and 8 dpi, representing infected leaf primordia and fully developed tumors, respectively. At 4 and 8 dpi, we observed a substantial increase in contents of the nitrogen-rich amino acids glutamine and asparagine, while the activities of enzymes involved in primary nitrogen assimilation and the content of ammonia and nitrate were reduced by 50% in tumors compared with mock controls. Employing stable isotope labeling, we could demonstrate that U. maydis-induced tumors show a reduced assimilation of soil-derived (15)NO(3)(-) and represent strong sinks for nitrogen. Specific labeling of the free amino acid pool of systemic source leaves with [(15)N]urea revealed an increased import of organic nitrogen from systemic leaves to tumor tissue, indicating that organic nitrogen provision supports the formation of U. maydis-induced tumors. In turn, amino acid export from systemic source leaves was doubled in infected plants. The analysis of the phloem amino acid pool revealed that glutamine and asparagine are not transported to the tumor tissue, although these two amino acids were found to accumulate within the tumor. Photosynthesis was increased and senescence was delayed in systemic source leaves upon tumor development on infected plants, indicating that the elevated sink demand for nitrogen could determine photosynthetic rates in source leaves.
Highlights
The basidiomycete Ustilago maydis is the causal agent of corn smut disease and induces tumor formation during biotrophic growth in its host maize (Zea mays)
We have conducted a combined transcriptome and metabolome analysis of infected leaf tissue at different time points after infection. Based on this data set, we previously described that U. maydis achieves a swift suppression of defense-related genes during the interaction and that photosynthetic gene expression is progressively reduced in infected leaves (Doehlemann et al, 2008a)
While extensive work has been done on nutrient acquisition and metabolism of the individual pathogens, only a few studies have addressed the question how overall host nitrogen metabolism is affected upon infection with biotrophic fungi
Summary
The basidiomycete Ustilago maydis is the causal agent of corn smut disease and induces tumor formation during biotrophic growth in its host maize (Zea mays). The causal agent of corn smut disease, is a biotrophic basidiomycete parasitizing maize (Zea mays) and its natural ancestor teosinte It can induce the formation of tumors on all aerial organs (Banuett, 1995), resulting in stunted growth and yield losses (Martinez-Espinoza et al, 2002). In infections by smut fungi, the plant plasma membrane gets invaginated and encases the growing hyphae (Doehlemann et al, 2009) This generates the so-called biotrophic interface, a compartment where fungal secretion leads to the formation of a vesicular matrix that comprises the enlarged contact zone typically found for members of the Ustilaginomycetes (Bauer et al, 1997; Begerow et al, 2006).
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