Evaluating plant growth–defense trade-offs by modelingthe interaction between primary and secondary metabolism

Understanding the molecular mechanisms behind plant response to stress can enhancebreeding strategies and help us design crop varieties with improved stress tolerance,yield, and quality. To investigate resource redistribution from growth- to defense-relatedprocesses in an essential tuber crop, potato, here we generate a large-scale compartmen-talized genome-scale metabolic model (GEM), potato-GEM. Apart from a large-scalereconstruction of primary metabolism, the model includes the full known potato sec-ondary metabolism, spanning over 566 reactions that facilitate the biosynthesis of 182distinct potato secondary metabolites. Constraint-based modeling identifies that theactivation of the largest amount of secondary (defense) pathways occurs at a decreaseof the relative growth rate of potato leaf, due to the costs incurred by defense. We thenobtain transcriptomics data from experiments exposing potato leaves to two bioticstress scenarios, a herbivore and a viral pathogen, and apply them as constraints toproduce condition-specific models. We show that these models recapitulate experimen-tally observed decreases in relative growth rates under treatment as well as changes inmetabolite levels between treatments, enabling us to pinpoint the metabolic rewiringunderlying growth–defense trade-offs. Potato- GEM thus presents a useful resource tostudy and broaden our understanding of potato and general plant defense responsesunder stress conditions.