Turning a plant tissue into a living cell froth through isotropic growth

The forms resulting from growth processes are highly sensitive to the nature of the driving impetus, and to the local properties of the medium, in particular, its isotropy or anisotropy. In turn, these local properties can be organized by growth. Here, we consider a growing plant tissue, the shoot apical meristem of Arabidopsis thaliana. In plants, the resistance of the cell wall to the growing internal turgor pressure is the main factor shaping the cells and the tissues. It is well established that the physical properties of the walls depend on the oriented deposition of the cellulose microfibrils in the extracellular matrix or cell wall; this order is correlated to the highly oriented cortical array of microtubules attached to the inner side of the plasma membrane. We used oryzalin to depolymerize microtubules and analyzed its influence on the growing meristem. This had no short-term effect, but it had a profound impact on the cell anisotropy and the resulting tissue growth. The geometry of the cells became similar to that of bubbles in a soap froth. At a multicellular scale, this switch to a local isotropy induced growth into spherical structures. A theoretical model is presented in which a cellular structure grows through the plastic yielding of its walls under turgor pressure. The simulations reproduce the geometrical properties of a normal tissue if cell division is included. If not, a "cell froth" very similar to that observed experimentally is obtained. Our results suggest strong physical constraints on the mechanisms of growth regulation.