Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis

Here, we describe our updated mathematical model of Arabidopsis thaliana Columbia metabolism, which adds the glucosinolates, an important group of secondary metabolites, to the reactions of primary metabolism. In so doing, we also describe the evolutionary origins of the enzymes involved in glucosinolate synthesis. We use this model to address a long-standing question in plant evolutionary biology: whether or not apparently defensive compounds such as glucosinolates are metabolically costly to produce. We use flux balance analysis to estimate the flux through every metabolic reaction in the model both when glucosinolates are synthesized and when they are absent. As a result, we can compare the metabolic costs of cell synthesis with and without these compounds, as well as inferring which reactions have their flux altered by glucosinolate synthesis. We find that glucosinolate production can increase photosynthetic requirements by at least 15% and that this cost is specific to the suite of glucosinolates found in A. thaliana, with other combinations of glucosinolates being even more costly. These observations suggest that glucosinolates have evolved, and indeed likely continue to evolve, for herbivory defense, since only this interpretation explains the maintenance of such costly traits.