Metabolic engineering of plants can reduce the cost and environmental impact of agriculture while providing for the needs of a growing population. Although our understanding of plant metabolism continues to increase at a rapid pace, relatively few plant metabolic engineering projects with commercial potential have emerged, in part because of a lack of principles for the rational manipulation of plant phenotype. One underexplored approach to identifying such design principles derives from analysis of the dominant constraints on plant fitness, and the evolutionary innovations in response to those constraints, that gave rise to the enormous diversity of natural plant metabolic pathways.