Dissection of the Complex Transcription and Metabolism Regulation Networks Associated with Maize Resistance to Ustilago maydis

The biotrophic fungal pathogen Ustilago maydis causes common smut in maize, forming tumors on all aerial organs, especially on reproductive organs, leading to significant reduction in yield and quality defects. Resistance to U. maydis is thought to be a quantitative trait, likely controlled by many minor gene effects. However, the genes and the underlying complex mechanisms for maize resistance to U. maydis remain largely uncharacterized. Here, we conducted comparative transcriptome and metabolome study using a pair of maize lines with contrast resistance to U. maydis post-infection. WGCNA of transcriptome profiling reveals that defense response, photosynthesis, and cell cycle are critical processes in maize response to U. maydis, and metabolism regulation of glycolysis, amino acids, phenylpropanoid, and reactive oxygen species are closely correlated with defense response. Metabolomic analysis supported that phenylpropanoid and flavonoid biosynthesis was induced upon U. maydis infection, and an obviously higher content of shikimic acid, a key compound in glycolysis and aromatic amino acids biosynthesis pathways, was detected in resistant samples. Thus, we propose that complex gene co-expression and metabolism networks related to amino acids and ROS metabolism might contribute to the resistance to corn smut.

Automated summary

This study found that defense response, photosynthesis, and cell cycle are critical processes in maize response to the biotrophic fungal pathogen Ustilago maydis, and metabolism regulation of glycolysis, amino acids, phenylpropanoid, and reactive oxygen species are closely correlated with defense response. Metabolomic analysis supported that certain biosynthesis pathways were induced upon U. maydis infection, and a higher content of key compounds in certain pathways were detected in resistant samples, indicating the complex gene co-expression and metabolism networks might contribute to the resistance to corn smut.