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A global regulation inducing the shape of growing folded leaves.

ABSTRACT: Shape is one of the important characteristics for the structures observed in living organisms. Whereas biologists have proposed models where the shape is controlled on a molecular level [1], physicists, following Turing [2] and d'Arcy Thomson [3], have developed theories where patterns arise spontaneously [4]. Here, we propose that volume constraints restrict the possible shapes of leaves. Focusing on palmate leaves (with lobes), the central observation is that developing leaves first grow folded inside a bud, limited by the previous and subsequent leaves. We show that the lobe perimeters end at the border of this small volume. This induces a direct relationship between the way it was folded and the final unfolded shape of the leaf. These dependencies can be approximated as simple geometrical relationships that we confirm on both folded embryonic and unfolded mature leaves. We find that independent of their position in the phylogenetic tree, these relationships work for folded species, but do not work for non-folded species. This global regulation for the leaf growth could come from a mechanical steric constraint. Such steric regulation should be more general and considered as a new simple means of global regulation.

SUBMITTER: Couturier E

PROVIDER: S-EPMC2776983 | biostudies-literature | 2009 Nov

REPOSITORIES: biostudies-literature

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A global regulation inducing the shape of growing folded leaves.

Couturier Etienne E Courrech du Pont Sylvain S Douady Stéphane S

PloS one 20091123 11

Shape is one of the important characteristics for the structures observed in living organisms. Whereas biologists have proposed models where the shape is controlled on a molecular level [1], physicists, following Turing [2] and d'Arcy Thomson [3], have developed theories where patterns arise spontaneously [4]. Here, we propose that volume constraints restrict the possible shapes of leaves. Focusing on palmate leaves (with lobes), the central observation is that developing leaves first grow folde ...[more]

PMID: 19956690

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Project description:The spatial gradient of signaling molecules is pivotal for establishing developmental patterns of multicellular organisms. It has long been proposed that these gradients could arise from the pure diffusion process of signaling molecules between cells, but whether this simplest mechanism establishes the formation of the tissue-scale gradient remains unclear. Plasmodesmata are unique channel structures in plants that connect neighboring cells for molecular transport. In this study, we measured cellular- and tissue-scale kinetics of molecular transport through plasmodesmata in Arabidopsis thaliana developing leaf primordia by fluorescence recovery assays. These trans-scale measurements revealed biophysical properties of diffusive molecular transport through plasmodesmata and revealed that the tissue-scale diffusivity, but not the cellular-scale diffusivity, is spatially different along the leaf proximal-to-distal axis. We found that the gradient in cell size along the developmental axis underlies this spatially different tissue-scale diffusivity. We then asked how this diffusion-based framework functions in establishing a signaling gradient of endogenous molecules. ANGUSTIFOLIA3 (AN3) is a transcriptional co-activator, and as we have shown here, it forms a long-range signaling gradient along the leaf proximal-to-distal axis to determine a cell-proliferation domain. By genetically engineering AN3 mobility, we assessed each contribution of cell-to-cell movement and tissue growth to the distribution of the AN3 gradient. We constructed a diffusion-based theoretical model using these quantitative data to analyze the AN3 gradient formation and demonstrated that it could be achieved solely by the diffusive molecular transport in a growing tissue. Our results indicate that the spatially different tissue-scale diffusivity is a core mechanism for AN3 gradient formation. This provides evidence that the pure diffusion process establishes the formation of the long-range signaling gradient in leaf development.

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A global regulation inducing the shape of growing folded leaves.

Publications

A global regulation inducing the shape of growing folded leaves.

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