How organs reach their final shape is a central yet unresolved question in developmental biology. Here we investigate whether mechanical cues contribute to this process. We analyze the epidermal cells of the Arabidopsis sepal, focusing on cortical microtubule arrays, which align along maximal tensile stresses and restrict growth in that direction through their indirect impact on the mechanical anisotropy of cell walls. We find a good match between growth and microtubule orientation throughout most of the development of the sepal. However, at the sepal tip, where organ maturation initiates and growth slows down in later stages, microtubules remain in a configuration consistent with fast anisotropic growth, i.e., transverse, and the anisotropy of their arrays even increases. To understand this apparent paradox, we built a continuous mechanical model of a growing sepal. The model demonstrates that differential growth in the sepal can generate transverse tensile stress at the tip. Consistently, microtubules respond to mechanical perturbations and align along maximal tension at the sepal tip. Including this mechanical feedback in our growth model of the sepal, we predict an impact on sepal shape that is validated experimentally using mutants with either increased or decreased microtubule response to stress. Altogether, this suggests that a mechanical feedback loop, via microtubules acting both as stress sensor and growth regulator, channels the growth and shape of the sepal tip. We propose that this proprioception mechanism is a key step leading to growth arrest in the whole sepal in response to its own growth.

A landmark of developmental biology is the production of reproducible shapes, through stereotyped morphogenetic events. At the cell level, growth is often highly heterogeneous, allowing shape diversity to arise. Yet, how can reproducible shapes emerge from such growth heterogeneity? Is growth heterogeneity filtered out? Here, we focus on rapidly growing trichome cells in the Arabidopsis sepal, a reproducible floral organ. We show via computational modeling that rapidly growing cells may distort organ shape. However, the cortical microtubule alignment along growth-derived maximal tensile stress in adjacent cells would mechanically isolate rapidly growing cells and limit their impact on organ shape. In vivo, we observed such microtubule response to stress and consistently found no significant effect of trichome number on sepal shape in wild-type and lines with trichome number defects. Conversely, modulating the microtubule response to stress in katanin and spiral2 mutant made sepal shape dependent on trichome number, suggesting that, while mechanical signals are propagated around rapidly growing cells, the resistance to stress in adjacent cells mechanically isolates rapidly growing cells, thus contributing to organ shape reproducibility.