Transcriptomic and metabolomic analyses unveil TaASMT3-mediated wheat resistance against stripe rust by promoting melatonin biosynthesis

Abstract

Plants have evolved a series of complicated defense mechanisms to counteract pathogen invasions. Although many studies have provided molecular evidence of resistance proteins and downstream signal transduction networks, the mechanisms by which plants resist pathogens remain poorly understood at the metabolite level. Here, we performed transcriptomic analyses of wheat leaves infected with Puccinia striiformis f. sp. tritici (Pst), the causal agent of wheat stripe rust. Functional enrichment analysis of identified differentially expressed genes (DEGs) revealed the strongest resistance responses at 24 h post-inoculation (hpi) in the incompatible wheat–Pst interaction system. Integrated with the metabolomics data at 24 hpi, we found that the amino acid metabolic pathways appeared to be directly involved in stripe rust resistance. Among these, five differentially abundant metabolites (DAMs) indole, tryptophan, tryptamine, N-Methylserotonin, and 5-Methoxyindoleacetate were enriched to the biosynthesis pathway of melatonin, a branch of tryptophan metabolism. Subsequent UPLC-MS/MS analysis confirmed that melatonin was highly accumulated in the incompatible wheat–Pst system, but not in the compatible interaction system. Exogenous melatonin treatment induced wheat resistance to Pst. The most significantly upregulated melatonin biosynthesis-related gene in the incompatible wheat–Pst system was TaASMT3, which encodes an acetylserotonin O-methyltransferase. Virus-induced gene silencing analysis revealed that knocking down TaASMT3 reduced wheat resistance to stripe rust, further suggesting a positive role of melatonin in wheat resistance to Pst. Taken together, these data suggest that melatonin was accumulated during Pst infection to activate wheat defense responses, offering a new perspective for elucidation of wheat stripe rust resistance based on metabolic dynamics.