Abstract
Differentiation into well-defined patterns and tissue growth are recognized as key processes in organismal development. However, it is unclear whether patterns are passively, homogeneously dilated by growth or whether they remodel during tissue expansion. Leaf vascular networks are well-fitted to investigate this issue, since leaves are approximately two-dimensional and grow manyfold in size. Here we study experimentally and computationally how vein patterns affect growth. We first model the growing vasculature as a network of viscoelastic rods and consider its response to external mechanical stress. We use the so-called texture tensor to quantify the local network geometry and reveal that growth is heterogeneous, resembling non-affine deformations in composite materials. We then apply mechanical forces to growing leaves after veins have differentiated, which respond by anisotropic growth and reorientation of the network in the direction of external stress. External mechanical stress appears to make growth more homogeneous, in contrast with the model with viscoelastic rods. However, we reconcile the model with experimental data by incorporating randomness in rod thickness and a threshold in the rod growth law, making the rods viscoelastoplastic. Altogether, we show that the higher stiffness of veins leads to their reorientation along external forces, along with a reduction in growth heterogeneity. This process may lead to the reinforcement of leaves against mechanical stress. More generally, our work contributes to a framework whereby growth and patterns are coordinated through the differences in mechanical properties between cell types.
Highlights
Organismal development relies on both the progressive differentiation of cells according to specific spatial patterns and the growth of tissues and organs towards their target shapes
The development of an organism involves a coordination between the differentiation of cells in well-defined spatial patterns and the growth of tissues towards their target shapes
While extensive research has addressed each of these key processes, their coordination has PLOS Computational Biology | DOI:10.1371/journal.pcbi
Summary
Organismal development relies on both the progressive differentiation of cells according to specific spatial patterns and the growth of tissues and organs towards their target shapes. As growth entails dynamic changes in the structural elements that define shape, such as the cytoskeleton or the extra-cellular matrix, it is essential to address the physical properties of these elements and how these properties are controlled at the cellular level [9,10,11,12,13,14,15,16,17]. In this framework, cell mechanics would provide a direct link between biochemical activity and growth.
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