Comparative multi-omics uncover conserved and lineage-specific defense strategies to southern corn rust in temperate and tropical maize.

Temperate and tropical maize inbred lines achieve high-level resistance to southern corn rust through distinct ETI associated and PTI associated signaling networks, with the peroxidase gene PER1 functioning as a common positive regulator across both resistance types. Southern corn rust (SCR), caused by the fungus Puccinia polysora, is a devastating fungal disease that leads to significant yield losses in maize worldwide. This study employs an integrated multi-omics approach, combining phenotyping, transcriptomics, metabolomics, weighted gene co-expression network analysis (WGCNA), and gene silencing, to delineate the molecular mechanisms of SCR resistance in temperate (Temp_R, R241) and tropical (Tr_R, Nei50205) maize inbred lines. Both lines displayed stable, high-level resistance, with Tr_R exhibiting more rapid callose deposition and cell wall fortification. Multi-omics analysis revealed that both resistant lines share activation of jasmonic acid (JA) signaling as a common defense foundation. Temp_R showed a stronger reliance on JA signaling and an intracellular defense cascade mediated by ncRNA-EDR1-RPP13L3. In addition to the common JA foundation, Tr_R also activates pattern-triggered immunity (PTI) associated signatures via LRR-RLK/CRK40 kinases, which further potentiates cell wall reinforcement through phenylpropanoid metabolism. Furthermore, we identified the peroxidase gene PER1 as a common positive regulator of resistance in both lines. Our findings unveil both shared and distinct genetic pathways underlying SCR resistance and underscore the value of tropical germplasm in breeding for durable resistance.