Pathogen-mediated priming induces intergenerational immunity against spot blotch in wheat

Spot blotch, caused by Bipolaris sorokiniana, is one of the most destructive diseases of wheat (Triticum aestivum), particularly in warm and humid regions where yield losses may exceed 30–50%. Heavy dependence on fungicides is neither sustainable nor environmentally safe, creating an urgent need for innovative strategies to enhance crop resilience. Defense priming, a phenomenon in which prior exposure to a mild stimulus enables plants to mount faster and stronger defenses upon subsequent stress offers a promising alternative. Pathogens or pathogen-derived molecules such as PAMPs and effectors are known to serve as effective priming stimuli in plants. In this study, we hypothesized that attenuated spores of B. sorokiniana could act as a priming stimulus to enhance resistance against spot blotch in wheat. By applying a low-dose spore suspension, we sought to establish pathogen-mediated priming as a green vaccination strategy, wherein controlled pre-exposure to attenuated inoculum enhances inducible resistance without imposing detectable growth penalties. Priming significantly reduced disease severity, with primed plants (P + B) showing a 2.6-fold lower percent disease index compared to non-primed controls (B). Biochemical analyses revealed enhanced photosynthetic pigments (Chlorophyll a 2.6-fold, Chlorophyll b 3.3-fold, Carotenoids 1.56-fold), increased antioxidant defenses (Superoxide Dismutase 1.4-fold, Catalase 1.4-fold, and Ascorbate peroxidase 1.5-fold, ascorbic acid 2.8-fold, proline 1.6-fold), reduced lipid peroxidation (4.1-fold decrease), and higher phenolic content (1.8-fold) along with elevated PAL (1.9-fold) and POX (1.5-fold) activity. Yield traits also improved, including 1.4-fold higher spike number, 2.0-fold greater spikelet fertility, and a 1.2-fold increase in thousand grain weight (TGW). Strikingly, these benefits were transmitted to the F1 generation, demonstrating that pathogen-mediated defense priming can induce intergenerational immune priming (IGIP). Taken together, our findings establish pathogen-mediated green vaccination as a sustainable strategy to enhance wheat resilience and provide durable protection against spot blotch.