Feedback from Tissue Mechanics Self-Organizes Efficient Outgrowth of Plant Organ

Plant organ outgrowth superficially appears like the continuous mechanical deformation of a sheet of cells. Yet, how precisely cells as individual mechanical entities can act to morph a tissue reliably and efficiently into three dimensions during outgrowth is still puzzling, especially when cells are tightly connected as in plant tissue. In plants, the mechanics of cells within a tissue is particularly well-defined because individual cell growth is essentially the mechanical yielding of the cell wall in response to internal turgor pressure. Cell-wall stiffness is controlled by biological signaling, which is impacted by stresses, and hence, cell growth is observed to respond to mechanical stresses building up within a tissue. What is the role of the mechanical feedback during morphing of tissue in three dimensions? Here, we develop a three-dimensional vertex model to investigate tissue mechanics at the onset of organ outgrowth at the tip of a plant shoot. We find that organ height is primarily governed by the ratio of growth rates of faster-growing cells initiating the organ versus slower-growing cells surrounding them. Remarkably, the outgrowth rate is higher when cell growth responds to the tissue-wide mechanical stresses. Our quantitative analysis of simulation data shows that tissue mechanical feedback on cell growth can act via a twofold mechanism. First, the feedback guides patterns of cellular growth. Second, the feedback modifies the stress patterns on the cells, consequently amplifying and propagating growth anisotropies. This mechanism may allow plants to grow organs efficiently out of the meristem by reorganizing the cellular growth rather than inflating growth rates.