Ibrahim Cheddadi

Plant morphogenesis relies on dynamic growth deformations at the cell and tissue scales driven by osmotic fluxes. A mechanistic understanding of this phenomenon demands a physical framework that integrates cell imbibition, tissue mechanics and water fluxes, as well as their biophysical and molecular regulations, within a theory of plant active matter capturing the open-system and out-of-equilibrium properties of tissues. Building on historical insights into growth geometry, physics and mechanics, combined with recent experimental results, we outline the key challenges in modelling plant growth and propose steps towards a unified physical theory of plant morphogenesis, in which biological regulation, mechanical forces and water fluxes interact to shape biological form through the fundamental principles of living matter.

Plant morphogenesis relies on dynamic growth deformations at the cell and tissue scales driven by osmotic fluxes. A mechanistic understanding of this phenomenon demands a physical framework that integrates cell imbibition, tissue mechanics, and water fluxes, as well as their biophysical and molecular regulations, within a theory of plant active matter capturing the open-system and out-of-equilibrium properties of tissues. Building on historical insights into growth geometry, physics, and mechanics, combined with recent experimental results, we outline the key challenges in modelling plant growth and propose steps towards a unified physical theory of plant morphogenesis, in which biological regulation, mechanical forces, and water fluxes interact to shape biological form through the fundamental principles of living matter.

The growth of plants is a hydromechanical phenomenon in which cells enlarge by absorbing water, while their walls expand and remodel under turgor-induced tension. In multicellular tissues, where cells are mechanically interconnected, morphogenesis results from the combined effect of local cell growths, which reflects the action of heterogeneous mechanical, physical, and chemical fields, each exerting varying degrees of nonlocal influence within the tissue. To describe this process, we propose a physical field theory of plant growth. This theory treats the tissue as a poromorphoelastic body, namely a growing poroelastic medium, where growth arises from pressure-induced deformations and osmotically-driven imbibition of the tissue. From this perspective, growing regions correspond to hydraulic sinks, leading to the possibility of complex non-local regulations, such as water competition and growth-induced water potential gradients. More in general, this work aims to establish foundations for a mechanistic, mechanical field theory of morphogenesis in plants, where growth arises from the interplay of multiple physical fields, and where biochemical regulations are integrated through specific physical parameters.

In multicellular organisms, tissue outgrowth creates a new water sink, modifying local hydraulic patterns. Although water fluxes are often considered passive by-products of development, their contribution to morphogenesis remains largely unexplored. Here, we mapped cell volumetric growth across the shoot apex in Arabidopsis thaliana. We found that, as organs grow, a subpopulation of cells at the organ-meristem boundary shrinks. Growth simulations using a model that integrates hydraulics and mechanics revealed water fluxes and predicted a water deficit for boundary cells. In planta, a water-soluble dye preferentially allocated to fast-growing tissues and failed to enter the boundary domain. Cell shrinkage next to fast-growing domains was also robust to different growth conditions and different topographies. Finally, a molecular signature of water deficit at the boundary confirmed our conclusion. Taken together, we propose that the differential sink strength of emerging organs prescribes the hydraulic patterns that define boundary domains at the shoot apex.

Summary: 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.

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. Plant cells are surrounded by a rigid wall that prevents cell displacements and rearrangements as in animal tissues. Therefore, plant morphogenesis relies only on cell divisions, shape changes, and local modulation of growth rate. It has long been recognized that cell growth relies on the competition between osmosis that tends to attract water into the cells and wall mechanics that resists to it, but this interplay has never been fully explored in a multicellular model. The goal of this work is to analyze the theoretical consequences of this coupling. We show that the emergent behavior is rich and complex: among other findings, pressure and growth rate heterogeneities are predicted without any ad-hoc assumption; furthermore the model can display a new type of lateral inhibition based on fluxes that could complement and strengthen the efficiency of already known mechanisms such as cell wall loosening.