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PLoS Comput Biol. 2014 Jan;10(1):e1003410. doi: 10.1371/journal.pcbi.1003410. Epub 2014 Jan 9.

Stress and strain provide positional and directional cues in development.

Author information

1
Computational Biology & Biological Physics, Lund University, Lund, Sweden.
2
Computational Biology & Biological Physics, Lund University, Lund, Sweden ; Sainsbury Laboratory, Cambridge University, Cambridge, United Kingdom.

Abstract

The morphogenesis of organs necessarily involves mechanical interactions and changes in mechanical properties of a tissue. A long standing question is how such changes are directed on a cellular scale while being coordinated at a tissular scale. Growing evidence suggests that mechanical cues are participating in the control of growth and morphogenesis during development. We introduce a mechanical model that represents the deposition of cellulose fibers in primary plant walls. In the model both the degree of material anisotropy and the anisotropy direction are regulated by stress anisotropy. We show that the finite element shell model and the simpler triangular biquadratic springs approach provide equally adequate descriptions of cell mechanics in tissue pressure simulations of the epidermis. In a growing organ, where circumferentially organized fibers act as a main controller of longitudinal growth, we show that the fiber direction can be correlated with both the maximal stress direction and the direction orthogonal to the maximal strain direction. However, when dynamic updates of the fiber direction are introduced, the mechanical stress provides a robust directional cue for the circumferential organization of the fibers, whereas the orthogonal to maximal strain model leads to an unstable situation where the fibers reorient longitudinally. Our investigation of the more complex shape and growth patterns in the shoot apical meristem where new organs are initiated shows that a stress based feedback on fiber directions is capable of reproducing the main features of in vivo cellulose fiber directions, deformations and material properties in different regions of the shoot. In particular, we show that this purely mechanical model can create radially distinct regions such that cells expand slowly and isotropically in the central zone while cells at the periphery expand more quickly and in the radial direction, which is a well established growth pattern in the meristem.

PMID:
24415926
PMCID:
PMC3886884
DOI:
10.1371/journal.pcbi.1003410
[Indexed for MEDLINE]
Free PMC Article

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