Abstract
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.
Highlights
Plants have deployed a highly sophisticated innate immune system to perceive potentially dangerous microbes; pathogens have developed strategies to facilitate their own progression on host plants
Time-course transcriptome analysis using a pair of contrast lines showed that numerous maize genes were uniquely up-regulated or down-regulated during maize in response to U. maydis infection
Induced by U. maydis were related to plant defense to fugal, reactive oxygen species (ROS) regulation, and amino acid metabolism regulation, suggesting that this trait is likely controlled by multiple genes and complex mechanisms
Summary
Plants have deployed a highly sophisticated innate immune system to perceive potentially dangerous microbes; pathogens have developed strategies to facilitate their own progression on host plants. The roles of PCD in plant innate immunity largely rely on the living style of colonizing pathogens; e.g., PCD is beneficial to necrotrophic pathogen, but it enables the host to restrict the invasion of biotrophic pathogens. U. maydis infection can trigger host immune responses, including reactive oxygen species (ROS) production, protease activation, and salicylic acid signaling. Despite research progress on the interaction between maize and U. maydis, host genes and associated resistance strategies deployed by maize to achieve successful defense to U. maydis have not been fully identified and characterized. Maizeline-specific genes were found to be involved in U. maydis and maize interaction [20] Taken together, these findings indicate that the regulation of transcription reprogramming of host genes is critical for the biotrophic infection of U. maydis. The joint analysis of transcriptomics and metabolomics provided more detailed explanation of the genetic and molecular mechanisms underlying the complex resistance trait of corn common smut at both transcription and metabolism levels
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