Multiscale models in the biomechanics of plant growth

Plant growth occurs through the coordinated expansion of tightly adherent cells, driven by regulated softening of cell walls. It is an intrinsically multiscale process, with the integrated properties of multiple cell walls shaping the whole tissue. Multiscale models encode physical relationships to bring new understanding to plant physiology and development

Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments

A combination of osmotic treatments, micro-indentation with cellular force microscopy, and inverse finite-element modelling gives an estimate for both turgor pressure and cell wall elasticity in plant cell

Stress and Strain Provide Positional and Directional Cues in Development

<div><p>The morphogenesis of organs necessarily involves mechanical interactions and changes in mechanical properties of a tissue. A long standing question is how such changes are directed on a cellular scale while being coordinated at a tissular scale. Growing evidence suggests that mechanical cues are participating in the control of growth and morphogenesis during development. We introduce a mechanical model that represents the deposition of cellulose fibers in primary plant walls. In the model both the degree of material anisotropy and the anisotropy direction are regulated by stress anisotropy. We show that the finite element shell model and the simpler triangular biquadratic springs approach provide equally adequate descriptions of cell mechanics in tissue pressure simulations of the epidermis. In a growing organ, where circumferentially organized fibers act as a main controller of longitudinal growth, we show that the fiber direction can be correlated with both the maximal stress direction and the direction orthogonal to the maximal strain direction. However, when dynamic updates of the fiber direction are introduced, the mechanical stress provides a robust directional cue for the circumferential organization of the fibers, whereas the orthogonal to maximal strain model leads to an unstable situation where the fibers reorient longitudinally. Our investigation of the more complex shape and growth patterns in the shoot apical meristem where new organs are initiated shows that a stress based feedback on fiber directions is capable of reproducing the main features of in vivo cellulose fiber directions, deformations and material properties in different regions of the shoot. In particular, we show that this purely mechanical model can create radially distinct regions such that cells expand slowly and isotropically in the central zone while cells at the periphery expand more quickly and in the radial direction, which is a well established growth pattern in the meristem.</p></div

Growth and biomechanics of plant epidermal cells

Since plant cells are encased in rigid cell walls, approaching them as physical systems is necessary to fully understand the multi-level mechanisms controlling developmental processes. Therefore, in my thesis I tried to combine physical and biological methods to study the morphogenetic processes in the plant epidermis. I quantified growth of the Arabidopis thaliana sepal, an elliptical floral organ which is comprised of small, square cells and large, elongated ‘giant cells’ randomly interspersed between the small ones. I detected a wave of high anisotropic growth (growing predominantly in one direction): along the proximo-distal starting at the tip of the sepal, gradually moving to its base as the organ develops. Interestingly, replacing the giant cells with files of small cells (observed in the lgo mutant) does not change the overall growth rate tendencies. In contrast, the Arabidopsis cotyledon, which has a round shape, grows much more isotropically (at the same rate in all directions), even though its cells have very elaborate, jigsaw puzzle-like shapes. I used Cellular Force Microscopy (CFM) to measure stiffness (or, indirectly, turgor pressure) of sepal cells. A Finite Element Method (FEM) mechanical model showed that observed differences in measured stiffness values between small and giant cells can be explained by cell geometry. Furthermore, using osmotic treatments I demonstrated in vivo that the cell wall is softer in the fast-growing areas than in the slow-growing areas. By comparing osmotic treatment results in wild type and the ftsh4 mutant, I speculated that Reactive Oxygen Species play an important role in cell maturation by locally stiffening the cell wall. Finally, I focused on more complex cell shapes as I employed genetic engineering, cell growth and shape quantification and computational modelling to answer the question why epidermal cells in leaves and cotyledons make jigsaw puzzle-like shapes. Cell shapes are adjusted to growth direction according to self-enhancing growth restriction, as proven by a growing mechanical model. I proposed puzzle cells minimize mechanical stress on the cell wall and therefore prevent it from bursting or needing to introduce additional structural reinforcements. Finally, I demonstrated several lines of evidence that plants of different cell shape and size, as well as different species, have an active mechanism of keeping this stress low. Taken together, my results contribute to the understanding of the role of cell shape in the epidermal tissue. They also provide novel input on mechanical properties of the cell wall during growth supported by in vivo experiments performed using state-of-the-art biomechanical methods