Puzzle cell shape emerges from the interaction of growth with mechanical constraints

Abstract

Puzzle-shaped epidermal cells not only reduce mechanical stress during organ growth but also record the expansion history of the tissue in their outlines. By combining mechanical simulations with time-lapse imaging, we show that transitions from directional to isotropic expansion induce new lobes to form along the previous growth axis, and that switching the order of anisotropic and isotropic phases yields hybrid shapes that reliably preserve those transitions. In maize, model predictions and live imaging coincide precisely, and in Ara-bidopsis, final lobe patterns correlate more with growth history than with cell size alone. Ge-netic or pharmacological disruption of lobe formation constrains leaf expansion or drives compensatory elongation, which underscores a mechanical function. A broad survey of living and fossil vascular plants reveals that the mechanism to make puzzle-shaped cells is both widespread and developmentally plastic, suggesting that single snapshots of leaves can give insight into their growth history. Together, these findings demonstrate that puzzle cells trans-form cell geometry into a living record of how tissues grow.