The determination of leaf size on the basis of developmental traits

Summary Mature leaf area (LA) is a showcase of diversity – varying enormously within and across species, and associated with the productivity and distribution of plants and ecosystems. Yet, it remains unclear how developmental processes determine variation in LA. We introduce a mathematical framework pinpointing the origin of variation in LA by quantifying six epidermal ‘developmental traits’: initial mean cell size and number (approximating values within the leaf primordium), and the maximum relative rates and durations of cell proliferation and expansion until leaf maturity. We analyzed a novel database of developmental trajectories of LA and epidermal anatomy, representing 12 eudicotyledonous species and 52 Arabidopsis experiments. Within and across species, mean primordium cell number and maximum relative cell proliferation rate were the strongest developmental determinants of LA. Trade‐offs between developmental traits, consistent with evolutionary and metabolic scaling theory, strongly constrain LA variation. These include trade‐offs between primordium cell number vs cell proliferation, primordium mean cell size vs cell expansion, and the durations vs maximum relative rates of cell proliferation and expansion. Mutant and wild‐type comparisons showed these trade‐offs have a genetic basis in Arabidopsis. Analyses of developmental traits underlying LA and its diversification highlight mechanisms for leaf evolution, and opportunities for breeding trait shifts.