Integrated transcriptomic and metabolomic analysis reveals the central role of phenylpropanoid biosynthesis in pea resistance to powdery mildew

Pea powdery mildew severely reduces crop yield and quality, yet the dynamic molecular and metabolic regulatory networks underlying resistance differences between different pea varieties remain poorly understood. Here, we profiled the defense landscape of susceptible (Longwan 3) and resistant (Longwan 5) pea varieties across three infection stages (0, 3, and 6 days post-inoculation) via integrated transcriptomic and metabolomic analyses. Multi-omics data revealed pronounced differences in metabolic reconfiguration (1754 metabolites identified) and transcriptional reprogramming (34566 genes annotated) between the two pea cultivars. Integrated Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses of differentially expressed genes (DEGs) and differentially accumulated metabolites (DAMs) consistently identified the phenylpropanoid biosynthesis pathway as the core pathway driving powdery mildew resistance. The resistant variety exhibited sustained upregulation of key biosynthetic genes (e.g., phenylalanine ammonia-lyase and cinnamate 4-hydroxylase), which directly drove the accumulation of defensive metabolites including ferulic acid and sinapic acid. Although some gene-metabolite correlations were consistent, others (e.g., those involving β-glucosidase and peroxidase genes) reflected a complex, multi-layered regulatory network involving post-transcriptional regulation and metabolic feedback mechanisms. Our study advances our understanding of dynamic defense mechanisms in legumes, and offers novel molecular targets for enhancing powdery mildew resistance, as well as efficient markers for precision breeding of elite pea varieties.