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Simulating Turgor-Induced Stress Patterns in Multilayered Plant Tissues

  • Special Issue: Multiscale Modeling of Tissue Growth and Shape
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Abstract

The intertwining between mechanics and developmental biology is extensively studied at the shoot apical meristem of land plants. Indeed, plant morphogenesis heavily relies on mechanics; tissue deformations are fueled by turgor-induced forces, and cell mechanosensitivity plays a major regulatory role in this dynamics. Since measurements of forces in growing meristems are still out of reach, our current knowledge relies mainly on theoretical and numerical models. So far, these modeling efforts have been mostly focusing on the epidermis, where aerial organs are initiated. In many models, the epidermis is assimilated to its outermost cell walls and described as a thin continuous shell under pressure, thereby neglecting the inner walls. There is, however, growing experimental evidence suggesting a significant mechanical role of these inner walls. The aim of this work is to investigate the influence of inner walls on the mechanical homeostasis of meristematic tissues. To this end, we simulated numerically the effect of turgor-induced loading, both in realistic flower buds and in more abstract structures. These simulations were performed using finite element meshes with subcellular resolution. Our analysis sheds light on the mechanics of growing plants by revealing the strong influence of inner walls on the epidermis mechanical stress pattern especially in negatively curved regions. Our simulations also display some strong and unsuspected features, such as a correlation between stress intensity and cell size, as well as differential response to loading between epidermal and inner cells. Finally, we monitored the time evolution of the mechanical stresses felt by each cell and its descendants during the early steps of flower morphogenesis.

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Acknowledgements

The authors would like to thank: Guillaume Cerutti for his advice on mesh generation, Arezki Boudaoud and Olivier Hamant for their useful comments and also Jonathan Legrand and Pradeep Das for kindly providing the time series of segmented 3D images of the growing flower bud used in this analysis. The authors also thank Gabriella Mosca for informal discussions and comments on the work.

Funding

Funding was provided by European Research Council (Grant No. Morphodynamics) and Inria Project Lab (Grant No. Morphogenetics).

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Authors and Affiliations

  1. Laboratoire de Reproduction et Développement des plantes, Univ Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, Inria, 69342, Lyon, France

    Olivier Ali, Hadrien Oliveri, Jan Traas & Christophe Godin

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  1. Olivier Ali
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  2. Hadrien Oliveri
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  3. Jan Traas
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Correspondence to Olivier Ali.

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Ali, O., Oliveri, H., Traas, J. et al. Simulating Turgor-Induced Stress Patterns in Multilayered Plant Tissues. Bull Math Biol 81, 3362–3384 (2019). https://doi.org/10.1007/s11538-019-00622-z

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