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Open Access Research article

Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis: a dynamic spatial model

Mariana Benítez13, Carlos Espinosa-Soto14, Pablo Padilla-Longoria2 and Elena R Alvarez-Buylla13*

Author Affiliations

1 Instituto de Ecología, Universidad Nacional Autónoma de México, Ciudad Universitaria 3er Circuito Exterior, Junto Jardín Botánico Exterior, Coyoacán 04510, DF, Mexico

2 Instituto de Investigación en Matemáticas Aplicadas y Sistemas, Universidad Nacional Autónoma de México, DF, Mexico

3 Centro de Ciencias de la Complejidad, Ciudad Universitaria, DF, Mexico

4 Department of Biochemistry, University of Zurich, Switzerland

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BMC Systems Biology 2008, 2:98  doi:10.1186/1752-0509-2-98

Published: 17 November 2008

Abstract

Background

Dynamical models are instrumental for exploring the way information required to generate robust developmental patterns arises from complex interactions among genetic and non-genetic factors. We address this fundamental issue of developmental biology studying the leaf and root epidermis of Arabidopsis. We propose an experimentally-grounded model of gene regulatory networks (GRNs) that are coupled by protein diffusion and comprise a meta-GRN implemented on cellularised domains.

Results

Steady states of the meta-GRN model correspond to gene expression profiles typical of hair and non-hair epidermal cells. The simulations also render spatial patterns that match the cellular arrangements observed in root and leaf epidermis. As in actual plants, such patterns are robust in the face of diverse perturbations. We validated the model by checking that it also reproduced the patterns of reported mutants. The meta-GRN model shows that interlinked sub-networks contribute redundantly to the formation of robust hair patterns and permits to advance novel and testable predictions regarding the effect of cell shape, signalling pathways and additional gene interactions affecting spatial cell-patterning.

Conclusion

The spatial meta-GRN model integrates available experimental data and contributes to further understanding of the Arabidopsis epidermal system. It also provides a systems biology framework to explore the interplay among sub-networks of a GRN, cell-to-cell communication, cell shape and domain traits, which could help understanding of general aspects of patterning processes. For instance, our model suggests that the information needed for cell fate determination emerges from dynamic processes that depend upon molecular components inside and outside differentiating cells, suggesting that the classical distinction of lineage versus positional cell differentiation may be instrumental but rather artificial. It also suggests that interlinkage of nonlinear and redundant sub-networks in larger networks is important for pattern robustness. Pursuing dynamic analyses of larger (genomic) coupled networks is still not possible. A repertoire of well-characterised regulatory modules, like the one presented here, will, however, help to uncover general principles of the patterning-associated networks, as well as the peculiarities that originate diversity.