Why do plants make puzzle-shaped cells?

Many plant epidermal cells form interlocking shapes that look like jigsaw puzzle pieces. However, scientists have struggled to understand how these complex shapes benefit the plant. We proposed that the puzzle cell shape allows the plant to create large cells in the epidermis, preventing them from bulging out excessively under the high stresses caused by turgor pressure. We tested our hypothesis with a computer simulation model of the emergence of these intricate forms, based on the feedback between cell shape and mechanical stress.

HFSP Program Grant holders Olivier Hamant, Chun Biu Li, Adrienne Roeder and Richard Smith and colleagues
authored on Fri, 13 April 2018

Plant cells are encased in a rigid cell wall that must be able to withstand the high turgor pressure within the cell, a pressure that can be several times that of a car tire. The size and shape of a plant cell strongly influence the distribution of forces on the cell wall, in the same way as in man-made pressurized structures. A main difference, however, is that plant cells grow, expanding up to a hundred or more times their original size. In this study we performed Finite Element Method (FEM) computer simulations to examine distribution of mechanical stress in the cell wall and assessed how the cells may grow in order to not put too much stress on the wall. Lower stress means that less energy needs to be invested in building the cell wall, and would be advantageous for the plant. We found that the most convenient way is to expand only in one direction (in other words, to elongate or grow anisotropically) in order to avoid large open areas where the cells bulge out and the stress becomes very high. This strategy works for long thin structures such as root and stems, however plants also need to make a variety of different shapes like those found in the leaves and flowers. In these more isotropic organs, cells must grow in more than one direction, and the puzzle cell shape allows this while keeping mechanical stress low.

Figure: Visualization of the stresses in puzzle cells. Large open areas have the highest stress. (Colorbar MPa).

Since jigsaw puzzle-shaped cells are commonly seen in plants, there have been many attempts to explain how these intricate forms are created. Most of this work focuses on potential molecular pathways regulating cell shape, but it has remained unclear whether the mechanism is based on local growth enhancement in the lobes, growth restriction in the indentations, or a combination of the two. Since a lobe in one cell must fit into an indentation in its neighbor it has also been proposed that there must be some mobile chemical signal coordinating this process between cells. Here, we approached the problem from a mechanical perspective, and arrived at a model that not only addresses the “how”, but also the ”why”. We simulated a tissue of small cells with simple shape, and added growth. As the cells get larger the stress increases, growth restrictions are added to counteract large open areas that would bulge and have high stress. If growth is only in one direction, we get long thin cells, however when growth is isotropic, the puzzle shape emerges. The model predicts that cell shape, puzzle or not, depends on how the tissue grows. We then tested this prediction by looking at the correlation between growth and cell shape in several species and tissues, and found that the puzzle shape is indeed correlated with growth isotropy. Genetic manipulations that change growth isotropy also induced the predicted changes in cell shape.

This work resulted from close collaboration between the HFSP awardees’ labs. The first observation of correlation between isotropic growth and puzzle-like cell shape came from the Roeder Lab (Cornell University) and was then explored in collaboration with the Smith Lab (Max Planck Institute for Plant Breeding Research). The Hamant Lab (ENS de Lyon) provided experimental evidence that cells may explode due to high mechanical stress and the Li Lab (Hokkaido University/Stockholm University) provided the statistical analysis of cell shape within a wide range of plant species.

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Why plants make puzzle cells, and how their shape emerges. Sapala, A., Runions, A., Routier-Kierzkowska, A.L., Gupta, M.D., Hong, L., Hofhuis, H., Verger, S., Mosca, G., Li, C.B., Hay, A., Hamant, O., Roeder, A.H.K., Tsiantis, M., Prusinkiewicz, P., Smith, R.S. 2018. eLife, 7, p.e32794. DOI: 10.7554/eLife.32794

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