Integrated transcriptomics and metabolomics revealed the role of the flavonoid pathway in the resistance of Zanthoxylum bungeanum against leaf rust

• Five Z. bungeanum cultivars were evaluated the resistance against C. zanthoxyli . • Two cultivars (FD and QJ) were utilized to investigate the resistance mechanism through transcriptome and metabolome. • The flavonoid pathway plays a dominant role in the resistance of Z. bungeanum leaves against C. zanthoxyli . • In QJ, upon infection with C. zanthoxyli , the core genes and enzymes involved in the flavonoid pathway were upregulated. • The key flavonoids in the flavonoid pathway exhibiting strong inhibitory activity against the spore germination of C. zanthoxyli . Leaf rust caused by Coleosporium zanthoxyli is a destructive disease that threatens Zanthoxylum bungeanum plantations. To address this, screening for resistant cultivars and exploring their resistance mechanisms are crucial for effective disease management. However, the mechanisms underlying Z. bungeanum 's resistance remain unclear. In this study, we conducted in vivo and in vitro experiments to screen for the resistant cultivar Qiujiao (QJ) and the susceptible cultivar Fengxian Dahongpao (FD). Subsequently, the resistance mechanisms of Z. bungeanum were analyzed by integrating transcriptome and metabolome, the result showed the flavonoid pathway served as the primary metabolic pathway for QJ to confer resistance against C. zanthoxyli . Upon infection with C. zanthoxyli , the key genes ( PAL, CHI , and HCT ) and enzymes (PAL, C4H, and 4CL) involved in the flavonoid pathway were upregulated in QJ, and the total flavonoid content was increased in QJ. Additionally, eight flavonoids from this pathway demonstrated inhibitory effects on C. zanthoxyli spore germination, with naringenin and phloretin exhibiting the stronger activity. Collectively, the flavonoid pathway plays a dominant role in the resistance of Z. bungeanum leaves against C. zanthoxyli . By studying the differences in leaf rust resistance between two cultivars to reveal the accumulation of flavonoids is the main cause of resistance. In the flavonoid pathway, flavanones, chalcones, and flavones play crucial roles against leaf rust.