The determination of leaf size on the basis of developmental traits

Abstract

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• 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.