Transcriptomic and metabolomic analyses reveal early coordination between redox homeostasis and phenylpropanoid metabolism associated with oat resistance to Drechslera avenae

Abstract

Oat ( Avena sativa L.) is an important grain and forage crop, but oat leaf spot caused by Drechslera avenae ( D. avenae ) severely limits its production. However, the dynamic defense mechanisms underlying genotype-dependent resistance to this disease remain unclear. We characterized the temporal defense responses distinguishing a resistant and a susceptible oat cultivar during infection. Physiological responses (0–168 h post inoculation, hpi) and transcriptomic and metabolomic responses (0–120 hpi) of the resistant cultivar ‘Haymaker’ and the susceptible cultivar ‘Molasses’ were compared after D. avenae inoculation, complemented by an exogenous ascorbic acid application assay. ‘Molasses’ showed higher disease severity, hydrogen peroxide (H₂O₂), and malondialdehyde (MDA), whereas ‘Haymaker’ displayed faster early antioxidant responses, greater flavonoid accumulation, and stronger lignin-associated defense responses. The 12–24 hpi window was critical for defense divergence, with rapid induction of RLK , CaM , NLR , PTI1 , WRKY , and MAPK genes in ‘Haymaker’. Joint transcriptomic and metabolomic pathway analysis revealed earlier activation of the ascorbate–glutathione system ( OPLAH , GCL , GR , GST ) and stronger phenylpropanoid-associated metabolism ( PTAL , 4CL , CCR , POD ) in ‘Haymaker’. Exogenous ascorbic acid reduced disease severity and oxidative damage. Oat resistance to leaf spot is associated with the timely integration of immune perception, redox buffering, and phenylpropanoid-associated defense metabolism during the early infection stage. The 12–24 hpi interval represents a critical transition point at which resistant plants establish a more coordinated defense state, while exogenous ascorbate further supports the functional relevance of redox regulation in disease suppression. These findings provide candidate genes and temporal targets for breeding oat cultivars with improved resistance to leaf spot.