Why plants make puzzle cells, and how their shape emerges

The shape and function of plant cells are often highly interdependent. The puzzle-shaped cells that appear in the epidermis of many plants are a striking example of a complex cell shape, however their functional benefit has remained elusive. We propose that these intricate forms provide an effective strategy to reduce mechanical stress in the cell wall of the epidermis. When tissue-level growth is isotropic, we hypothesize that lobes emerge at the cellular level to prevent formation of large isodiametric cells that would bulge under the stress produced by turgor pressure. Data from various plant organs and species support the relationship between lobes and growth isotropy, which we test with mutants where growth direction is perturbed. Using simulation models we show that a mechanism actively regulating cellular stress plausibly reproduces the development of epidermal cell shape. Together, our results suggest that mechanical stress is a key driver of cell-shape morphogenesis.
eLife digest Cells with complex interlocking shapes, similar to pieces of a jigsaw puzzle, cover the surface of many leaves. Why do these curious shapes form, and what benefit do they provide to the plant? Plant cells are like small balloons surrounded by a strong cell wall. Their internal pressure can be higher than the pressure in a car tire. It is this pressure that gives non-woody plant tissue its shape. Take away the pressure, and the plant wilts. The pressure inside a cell creates a lot of mechanical stress on the epidermal cell walls – those that make up the surface of the plant. The extent of the stress depends on the shape and size of the cells; for example, large cells bulge out and experience more stress than small cells. This could mean that the shape of puzzle cells is an adaptation used by plants to reduce the stress on their surface. To investigate this possibility, Sapala, Runions et al. developed a computer simulation that models how a plant grows and re-creates a variety of realistic puzzle cell shapes. The simulations show that ‘paving’ the leaf surface with puzzle shaped cells instead of more regularly shaped cells reduces the stress in the epidermal cell walls. Counterintuitively, the simulations also show that complex puzzle shapes develop in parts of the plant that grow isotropically (uniformly in all directions), such as leaves. If a plant organ grows mostly in one direction, like in a root or stem, long thin cells are sufficient to reduce the stress on the epidermal cell wall. Sapala, Runions et al. tested this idea by analyzing the shape of organs and cells in many plant species and by genetically modifying growth directions in Arabidopsis thaliana plants. This confirmed that puzzle cell shape is related to both organ shape and how isotropically the plant grows. It had previously been proposed that mobile chemical signals passed between cells coordinate the process by which a lobe in one puzzle cell matches an indentation in its neighbor. However, the model developed by Sapala, Runions et al. does not require such chemical signaling. Instead, mechanical forces and the shape the puzzle cells themselves may transmit this information. Mechanical forces are known to have important effects on the shape and behavior of cells from other species too. For example, animal cells can develop into different cell types depending on the stiffness of the surface they are placed on. Now that Sapala, Runions et al. have highlighted that plant cell shapes also adapt to mechanical forces, further research is needed to uncover how these forces are sensed.