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Computational modeling of cell cycle activity and leaf development in Arabidopsis thaliana

Final Activity Report Summary - LEAFMORPHOSIM (Computational modeling of cell cycle activity and leaf development in Arabidopsis thaliana)

Plant science is evolving from a reductionist view on the function of individual genes or pathways, to an integrated systems biology approach that focuses on the dynamic interactions between genes, proteins and metabolites. How do these interact to produce, and affect the higher levels of organization, including cells, tissues, organs and the whole plant? Inversely, how do patterns and behaviours at the higher organisation levels feed back to the molecular level? Mathematical and computational modelling play a central role in this multi-scale systems biology approach. In this project, funded by a Marie Curie Intra-European fellowhip, we have developed a computer model of leaf development.

Leaves grow in a complicated interplay between cell division, cell expansion, and pattern formation. A crucial step is the formation of a transport system, which brings nutrients to the growing leaf and drains waste products. A classic idea of how leaf venation forms is that of canalisation. Auxin, a plant hormone, would flow from the tip of the developing leaf towards the leaf stalk and would gradually narrow down to discrete streams. The basic idea is that cells would produce more auxin transporters if they transport more auxin. This positive feedback between auxin flux and pumping capacity would 'carve out' veins from the tissue, just like a water carves out rivers from a landscape.

Recent molecular evidence has identified receptor for auxin, but how cells should measure the flux of auxin is still unknown. Do plants really require a molecular sensor for auxin flux to construct polar auxin transport channels? We set out to determine if it were possible to define a simple mechanism that produces auxin channels with cells only sensitive to auxin concentration.

Using the computer model, we identified a putative mechanism for vein formation that is consistent with the current molecular data. In this mechanism, a travelling wave of auxin moves from the leaf tip to the leaf base. Auxin is concentrated into a peak, which then stimulates the production of auxin pumps. The pumps polarise towards the next cells and pump it onwards. In this way the travelling waves leave behind trails of polarized cells that would then differentiate into the vascular system.

The long-term goal of this continuing project is to reconstruct how leaves develop in the interplay between patterned cell division and cell expansion, and the transport of auxin and other signalling molecules between cells.