Fusarium head blight (FHB) is primarily caused by Fusarium graminearum and severely reduces wheat yield, causing mycotoxin contamination in grains and derived products. F. graminearum-secreted chemical toxins stably accumulate in plant cells, disturbing host metabolic homeostasis. We determined the potential mechanisms underlying FHB resistance and susceptibility in wheat. Three representative wheat varieties (Sumai 3, Yangmai 158, and Annong 8455) were inoculated with F. graminearum and their metabolite changes were assessed and compared. In total, 365 differentiated metabolites were successfully identified. Amino acids and derivatives, carbohydrates, flavonoids, hydroxycinnamate derivatives, lipids, and nucleotides constituted the major changes in response to fungal infection. Changes in defense-associated metabolites, such as flavonoids and hydroxycinnamate derivatives, were dynamic and differed among the varieties. Nucleotide and amino acid metabolism and the tricarboxylic acid cycle were more active in the highly and moderately resistant varieties than in the highly susceptible variety. We demonstrated that two plant-derived metabolites, phenylalanine and malate, significantly suppressed F. graminearum growth. The genes encoding the biosynthetic enzymes for these two metabolites were upregulated in wheat spike during F. graminearum infection. Thus, our findings uncovered the metabolic basis of resistance and susceptibility of wheat to F. graminearum and provided insights into engineering metabolic pathways to enhance FHB resistance in wheat.

Fusarium head blight (FHB), caused mainly by the fungus Fusarium graminearum, is one of the most devastating diseases in wheat, which reduces the yield and quality of grain. Fusarium graminearum infection of wheat cells triggers dynamic changes of gene expression in both F. graminearum and wheat, leading to molecular interactions between pathogen and host. The wheat plant in turn activates immune signaling or host defense pathways against FHB. However, the mechanisms by which F. graminearum infects wheat varieties with different levels of host resistance are largely limited. In this study, we conducted a comparative analysis of the F. graminearum transcriptome in planta during the infection of susceptible and resistant wheat varieties at three timepoints. A total of 6,106 F. graminearum genes including those functioning in cell wall degradation, synthesis of secondary metabolites, virulence, and pathogenicity were identified during the infection of different hosts, which were regulated by hosts with different genetic backgrounds. Genes enriched with metabolism of host cell wall components and defense response processes were specifically dynamic during the infection with different hosts. Our study also identified F. graminearum genes that were specifically suppressed by signals derived from the resistant plant host. These genes may represent direct targets of the plant defense against infection by this fungus. Briefly, we generated databases of in planta-expressed genes of F. graminearum during infection of two different FHB resistance level wheat varieties, highlighted their dynamic expression patterns and functions of virulence, invasion, defense response, metabolism, and effector signaling, providing valuable insight into the interactions between F. graminearum and susceptible/resistant wheat varieties.