Graft-transmissible resistance of cherry pepper (Capsicum annuum var. cerasiforme) to powdery mildew (Leveillula taurica) is associated with elevated superoxide accumulation, NADPH oxidase activity and pathogenesis-related gene expression

We found that resistance to pepper powdery mildew (PM) (Leveillula taurica) develops in a sweet pepper (Capsicum annuum) cultivar ('Total') when grafted on a resistant cherry pepper (C. annuum var. cerasiforme) rootstock (cv. Szentesi). Resistance is manifested both towards PM symptoms and pathogen accumulation. In healthy, uninfected plants PM-resistance can be predicted by enhanced accumulation of the reactive oxygen species (ROS) superoxide (O-2(center dot-)) and activity of NADPH oxidase, the enzyme mainly responsible for pathogenesis-related superoxide generation. In L. taurica-inoculated PM-resistant 'Szentesi' high levels of superoxide and NADPH oxidase activity are sustained even 45 days after inoculation, as opposed to PM-susceptible 'Total'. This is also true for 'Total' grafted on resistant 'Szentesi' rootstocks, where PM resistance, enhanced superoxide production and NADPH oxidase activity is likely due to an unknown, graft-transmitted signal. To further elucidate the mechanisms of graft-transmissible PM-resistance we monitored expression of pathogenesis-related (PR) genes in healthy and infected plants. In healthy plants, expression of CaPR-1 is several times higher in leaves of PM-resistant pepper than in sensitive plants, while high expression of CaPR-2 (glucanase) does not entirely correlate with PM-resistance, being detectable only in PM-resistant 'Szentesi'. However, during advanced stages of PM-pathogenesis (45 DAI) expression of CaPR-1 and CaPR-2 is by far the highest in PM-susceptible 'Total'. Our results suggest that the direct biochemical cause of graft-transmissible PM-resistance in pepper is the enhanced accumulation of NADPH oxidase-generated superoxide. To our knowledge, this is the first report on the role of ROS (superoxide) in graft-transmissible, pathogen-specific disease resistance.