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Integrating modeling into plant systems biology: Applications to auxin-driven plant morphogenesis

Final Report Summary - PLANTSYSMODEL (Integrating modeling into plant systems biology: Applications to auxin-driven plant morphogenesis)

One of the most central questions in biology is how the genome translates to biological form and function. To address that question, traditionally molecular geneticists identified mutant plants with developmental or physiological defects, then cloned the gene and studied it in knock-out and overexpression lines. “-Omics” approaches have added a broader toolbox, ultimately producing a list of the biological system's components (proteins, genes, etc.) and their interactions.

Systems biology should be more than that. It should teach us how the system's components dynamically interact to form a functioning whole. Computer modeling helps us to reconstruct the biological mechanism, recognize functional modules (e.g. feedback loops, signal transducers, etc.), and unravel cross-talk between levels of organization (genes, proteins, cells, tissues, whole plants). Thus it helps identify gaps in our understanding of the system that will drive new experiments and suggest novel hypotheses.

The primary aim of the PLANTSYSMODEL project was to further elucidate the role of polar auxin transport in plant development using computational modeling. The project focused on developmental patterning of the leaf and the flower in Arabidopsis thaliana. A secondary aim was to deliver tools that allow experimental biologists to actively participate in modeling.

A central player in leaf and flower development is auxin, a phytohormone whose local accumulation and directed transport is crucial in plant developmental mechanisms, ranging from phyllotaxis and root growth to flower and leaf patterning. The molecular actors related to auxin signaling, and the signaling networks they form have been characterized relatively well. A range of studies have described the polar auxin flux patterns and expression patterns of auxin-related studies have described the polar auxin flux patterns and expression patterns of auxin-related genes in the leaf and during lateral root initiation in great detail. Nevertheless, we understand poorly what mechanisms link the two scales: how do individual cell dynamics drive tissue-level patterning and vice versa? The combination of a good understanding of individual cell behavior and of the patterning occurring at the level of the whole tissue, together with a poor understanding of the mechanistic link between the two, makes the leaf and flower systems extremely well suited for cell-based modeling studies.

During the initial Marie Curie Intra-European fellowship, we have proposed a travelling-wave model for formation of the leaf midvein (Merks et al., 2007). The model was fine-tuned by extending it with auxin influx carriers (AUX1); also we additional rules for cell differentiation for separation of the L1 layer and the deeper layers in the growing leaf. In parallel, PhD student Krzysztof Wabnik at the VIB Dept. Plant Systems Biology in Ghent with Prof. Jiri Friml has developed the alternative extracellular receptor-based polarization model for leaf venation patterning (Wabnik et al., 2010). The model features a detailed auxin transport model, including auxin transport within cell wall compartments, and proposes polarized activity of the extracellular auxin binding protein (ABP1) is responsible for polarizing auxin transport. Experimentally, PhD student Stijn Dhondt has elucidated the roles of SHORTROOT and SCARECROW cell cycle regulators in the Arabidopsis leaf (Dhondt et al., 2010); these results will be integrated into the computational model. In collaboration with Dr. Simon van Mourik and coworkers at Wageningen University we have developed a model for auxindriven patterning in the growing Arabidopsis floral meristem (Van Mourik et al., PLoS ONE, in press). A (side-)project on lignin biosynthesis in poplar has resulted in a publication in Plant Physiology (Parijs et al., 2010).