Ustilago maydis Infection Strongly Alters Organic Nitrogen Allocation in Maize and Stimulates Productivity of Systemic Source Leaves

• Published in: Plant physiology (Bethesda) Vol. 152; no. 1; pp. 293 - 308
• Main Authors: Horst, Robin J, Doehlemann, Gunther, Wahl, Ramon, Hofmann, Jörg, Schmiedl, Alfred, Kahmann, Regine, Kämper, Jörg, Sonnewald, Uwe, Voll, Lars M
• Format: Journal Article
• Language: English
• Published: Rockville, MD American Society of Plant Biologists 01.01.2010
• Subjects: Amino acid metabolism; Amino acids; Biological and medical sciences; Corn; Down-Regulation; Fundamental and applied biological sciences. Psychology; Infections; Leaves; Nitrates; Nitrates - metabolism; Nitrogen; Nitrogen - metabolism; Photosynthesis; Phytopathology. Animal pests. Plant and forest protection; Plant Diseases - microbiology; Plant Leaves - metabolism; Plant Leaves - microbiology; Plant physiology and development; Plants; PLANTS INTERACTING WITH OTHER ORGANISMS; Soil - analysis; Tumors; Ustilago; Ustilago - physiology; Zea mays - metabolism; Zea mays - microbiology; Productivity; Monocotyledones; Organic nitrogen; Zea mays; Plant pathogen; Plant leaf; Systemic; Cereal crop; Basidiomycota; Fungi; Infection; Ustilago maydis; Plant physiology; Gramineae; Angiospermae; Spermatophyta
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.109.147702

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 ¹⁵NO₃⁻ and represent strong sinks for nitrogen. Specific labeling of the free amino acid pool of systemic source leaves with [¹⁵N]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.