Revisiting the relationship between turgor pressure and plant cell growth.

Growth is central to plant morphogenesis. Plant cells are encased in rigid cell walls, and they must overcome physical confinement to grow to specific sizes and shapes. Cell wall tension and turgor pressure are the main mechanical components impacting plant cell growth. Cell wall mechanics has been the focus of most plant biomechanical studies, and turgor pressure was often considered as a constant and largely passive component. Nevertheless, it is increasingly accepted that turgor pressure plays a significant role in plant growth. Numerous theoretical and experimental studies suggest that turgor pressure can be both spatially inhomogeneous and actively modulated during morphogenesis. Here, we revisit the pressure-growth relationship by reviewing recent advances in investigating the interactions between cellular/tissular pressure and growth.

Cellular Heterogeneity in Pressure and Growth Emerges from Tissue Topology and Geometry.

Cell-to-cell heterogeneity prevails in many systems, as exemplified by cell growth, although the origin and function of such heterogeneity are often unclear. In plants, growth is physically controlled by cell wall mechanics and cell hydrostatic pressure, alias turgor pressure. Whereas cell wall heterogeneity has received extensive attention, the spatial variation of turgor pressure is often overlooked. Here, combining atomic force microscopy and a physical model of pressurized cells, we show that turgor pressure is heterogeneous in the Arabidopsis shoot apical meristem, a population of stem cells that generates all plant aerial organs. In contrast with cell wall mechanical properties that appear to vary stochastically between neighboring cells, turgor pressure anticorrelates with cell size and cell neighbor number (local topology), in agreement with the prediction by our model of tissue expansion, which couples cell wall mechanics and tissue hydraulics. Additionally, our model predicts two types of correlations between pressure and cellular growth rate, where high pressure may lead to faster- or slower-than-average growth, depending on cell wall extensibility, yield threshold, osmotic pressure, and hydraulic conductivity. The meristem exhibits one of these two regimes, depending on conditions, suggesting that, in this tissue, water conductivity may contribute to growth control. Our results unravel cell pressure as a source of patterned heterogeneity and illustrate links between local topology, cell mechanical state, and cell growth, with potential roles in tissue homeostasis.

Coupling water fluxes with cell wall mechanics in a multicellular model of plant development.

The growth of plant organs is a complex process powered by osmosis that attracts water inside the cells; this influx induces simultaneously an elastic extension of the walls and pressure in the cells, called turgor pressure; above a threshold, the walls yield and the cells grow. Based on Lockhart's seminal work, various models of plant morphogenesis have been proposed, either for single cells, or focusing on the wall mechanical properties. However, the synergistic coupling of fluxes and wall mechanics has not yet been fully addressed in a multicellular model. This work lays the foundations of such a model, by simplifying as much as possible each process and putting emphasis on the coupling itself. Its emergent properties are rich and can help to understand plant morphogenesis. In particular, we show that the model can display a new type of lateral inhibitory mechanism that amplifies growth heterogeneities due e.g to cell wall loosening.

Integrating Physiology and Architecture in Models of Fruit Expansion.

Architectural properties of a fruit, such as its shape, vascular patterns, and skin morphology, play a significant role in determining the distributions of water, carbohydrates, and nutrients inside the fruit. Understanding the impact of these properties on fruit quality is difficult because they develop over time and are highly dependent on both genetic and environmental controls. We present a 3D functional-structural fruit model that can be used to investigate effects of the principle architectural properties on fruit quality. We use a three step modeling pipeline in the OpenAlea platform: (1) creating a 3D volumetric mesh representation of the internal and external fruit structure, (2) generating a complex network of vasculature that is embedded within this mesh, and (3) integrating aspects of the fruit's function, such as water and dry matter transport, with the fruit's structure. We restrict our approach to the phase where fruit growth is mostly due to cell expansion and the fruit has already differentiated into different tissue types. We show how fruit shape affects vascular patterns and, as a consequence, the distribution of sugar/water in tomato fruit. Furthermore, we show that strong interaction between tomato fruit shape and vessel density induces, independently of size, an important and contrasted gradient of water supply from the pedicel to the blossom end of the fruit. We also demonstrate how skin morphology related to microcracking distribution affects the distribution of water and sugars inside nectarine fruit. Our results show that such a generic model permits detailed studies of various, unexplored architectural features affecting fruit quality development.

Gap geometry dictates epithelial closure efficiency.

Closure of wounds and gaps in tissues is fundamental for the correct development and physiology of multicellular organisms and, when misregulated, may lead to inflammation and tumorigenesis. To re-establish tissue integrity, epithelial cells exhibit coordinated motion into the void by active crawling on the substrate and by constricting a supracellular actomyosin cable. Coexistence of these two mechanisms strongly depends on the environment. However, the nature of their coupling remains elusive because of the complexity of the overall process. Here we demonstrate that epithelial gap geometry in both in vitro and in vivo regulates these collective mechanisms. In addition, the mechanical coupling between actomyosin cable contraction and cell crawling acts as a large-scale regulator to control the dynamics of gap closure. Finally, our computational modelling clarifies the respective roles of the two mechanisms during this process, providing a robust and universal mechanism to explain how epithelial tissues restore their integrity.

Mechanics of epithelial closure over non-adherent environments.

The closure of gaps within epithelia is crucial to maintain its integrity during biological processes such as wound healing and gastrulation. Depending on the distribution of extracellular matrix, gap closure occurs through assembly of multicellular actin-based contractile cables or protrusive activity of border cells into the gap. Here we show that the supracellular actomyosin contractility of cells near the gap edge exerts sufficient tension on the surrounding tissue to promote closure of non-adherent gaps. Using traction force microscopy, we observe that cell-generated forces on the substrate at the gap edge first point away from the centre of the gap and then increase in the radial direction pointing into the gap as closure proceeds. Combining with numerical simulations, we show that the increase in force relies less on localized purse-string contractility and more on large-scale remodelling of the suspended tissue around the gap. Our results provide a framework for understanding the assembly and the mechanics of cellular contractility at the tissue level.