Integrative Transcriptomic and Metabolomic Analysis Reveals the Molecular Regulatory Mechanisms of Leaf Rust Resistance in Zanthoxylum armatum

Abstract

Simple Summary Zanthoxylum armatum is an economically important tree species in Southwest China valued for the flavor and medicinal properties of its fruits and leaves. Leaf rust disease severely threatens its cultivation. We discovered a spontaneous branch mutant with strong rust resistance on an otherwise susceptible individual. In this study, the resistant mutant (R-YF) and susceptible material (S-YF) were compared via physiological detection and metabolome and transcriptome analyses. The resistant mutant accumulated greater amounts of lignin for cell wall reinforcement, alongside higher levels of antifungal flavonoids. Vitexin, rutin, hyperoside, hydroxy-α-sanshool, hydroxy-β-sanshool, and hydroxy-γ-sanshool were significantly enriched in R-YF leaves. The AP2/ERF transcription factor family was identified as key regulators mediating defense responses. The resistant mutant achieves rust resistance by strengthening physical defense through cell wall reinforcement and by enhancing chemical defense through the accumulation of antimicrobial metabolites, under the control of AP2/ERF members. This research elucidates the molecular basis of natural rust resistance and supplies candidate targets for Zanthoxylum armatum disease-resistance breeding.