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

Abstract

AbstractThe puzzle-shaped cells found in the shoot epidermis of many plant species are a fascinating example of complex cell shapes. Because biological form often follows function, the unique shape of these cells suggests that they must serve some adaptive purpose for the plant. We previously proposed that these intricate shapes provide an effective strategy for reducing mechanical stress on the cell wall when epidermal cells undergo growth in more than one direction. Here we analyze a large selection of living and paleo plant species and find that the ability to make puzzle cells is a shared feature across all plant species, although their presence can be hidden as it varies depending on the organ, developmental stage, and environmental conditions. Computational modeling ofArabidopsisand maize epidermal cells revealed that presence and patterning of lobes is a dynamic process that is intricately linked to the growth history and environmental context of the plant organ. Conversely, disrupted lobeyness in mutants or with drug treatments affects plant development and leads to compensatory strategies. We propose that the mechanism underlying the formation of puzzle-shaped cells is likely conserved among higher plants and is a response to a developmental constraint driven by growth and mechanical stress.