Growth history leaves a geometric trace in puzzle cells

Puzzle-shaped epidermal cells can reduce mechanical stress during organ growth and, as shown here, can also record tissue expansion history in their outlines. By combining mechanical simulations with time-lapse imaging, we find that transitions from directional to isotropic expansion induce new lobes along the previous growth axis, and that reversing the sequence of anisotropic and isotropic phases yields hybrid shapes that preserve the sequence of growth phases. In maize, model predictions closely match live imaging, and in Arabidopsis, final lobe patterns correlate more strongly with growth history than with cell size alone. Genetic or pharmacological perturbations that reduce lobing are associated with constrained leaf expansion or compensatory elongation, consistent with a mechanical role. A broad survey of living and fossil vascular plants indicates that the capacity to form puzzle-shaped cells is widespread and developmentally plastic, suggesting that single snapshots of leaves can reflect prior growth dynamics across species. Together, these findings show that puzzle cells transform cell geometry into a living record of how tissues grow.