Downregulation of polyphenol oxidase in potato tubers redirects phenylpropanoid metabolism enhancing chlorogenate content and late blight resistance

Land plants synthesize phenolic compounds involved in plant defense against invading pathogens through the phenylpropanoid pathway. Although not considered as part of the phenylpropanoid pathway, plant polyphenol oxidases (PPOs) are enzymes that catalyze cresolase and catecholase reactions on several phenolic compounds. Here, transgenic potato (Solanum tuberosum) tubers with downregulated PPO genes (-PPO) were challenged with the oomycete pathogen Phytophthora infestans to investigate the interactions between PPO, phenylpropanoid metabolism, and disease resistance. We found that pathogen invasiveness was reduced in -PPO lines, while microscopic evidences suggested that the mechanism underlying the defense response involved the participation of phenolic compounds. Detailed metabolite-profiling analyses demonstrated that the concentration of metabolites related to the phenylpropanoid pathway and chlorogenate in particular was largely altered in PPO-downregulated tubers. Silencing of PPO caused a shift in metabolism from phenylpropanoid precursors to downstream phenylpropanoid products. The presented results suggest that downregulation of PPO redirects the phenylpropanoid metabolism leading to the accumulation of defensive phenolic compounds in the plant cells, consequently enhancing resistance to the pathogen. These results emphasize the importance of components acting in parallel to canonical metabolic pathway constituents in influencing plant metabolism and reveal new scenarios for modulating the levels of phenolics in crops.