A Gene Regulatory Network Model for Cell-Fate Determination duringArabidopsis thalianaFlower Development That Is Robust and Recovers Experimental Gene Expression Profiles[W]

Abstract

Flowers are icons in developmental studies of complex structures. The vast majority of 250,000 angiosperm plant species have flowers with a conserved organ plan bearing sepals, petals, stamens, and carpels in the center. The combinatorial model for the activity of the so-called ABC homeotic floral genes has guided extensive experimental studies in Arabidopsis thaliana and many other plant species. However, a mechanistic and dynamical explanation for the ABC model and prevalence among flowering plants is lacking. Here, we put forward a simple discrete model that postulates logical rules that formally summarize published ABC and non-ABC gene interaction data for Arabidopsis floral organ cell fate determination and integrates this data into a dynamic network model. This model shows that all possible initial conditions converge to few steady gene activity states that match gene expression profiles observed experimentally in primordial floral organ cells of wild-type and mutant plants. Therefore, the network proposed here provides a dynamical explanation for the ABC model and shows that precise signaling pathways are not required to restrain cell types to those found in Arabidopsis, but these are rather determined by the overall gene network dynamics. Furthermore, we performed robustness analyses that clearly show that the cell types recovered depend on the network architecture rather than on specific values of the model's gene interaction parameters. These results support the hypothesis that such a network constitutes a developmental module, and hence provide a possible explanation for the overall conservation of the ABC model and overall floral plan among angiosperms. In addition, we have been able to predict the effects of differences in network architecture between Arabidopsis and Petunia hybrida.

Coordination of plant cell division and expansion in a simple morphogenetic system

“…To properly understand the workings of such complex morphogenetic systems, it is necessary to construct dynamic models that contain an explicit description of these interactions. Though substantial progress has been made in the experimental description of the genetic processes that underlie plant morphogenesis (14,29), these are often poorly integrated with physical aspects of cellular growth. Current models have focused on patterning processes in plants (13,15), but have difficulty describing the establishment of biological shapes, because most models fail to consider the physical basis of growth adequately.…”

“…In previous studies, image analysis tools have been used to process microscopy images and quantify deformation in tissues (11,12). Software models based on reaction diffusion systems have been used to describe molecular transport phenomena (13), gene regulatory networks have been employed to model the regulation of gene expression (14), and feedback-regulated models for polar auxin transport can predict canalisation of vascular tissues (15). However, the mechanics of cell expansion is central to the regulation of cell shape and division, and there has been little focus on the physics of cellular growth within tissues.…”

Network Inference, Analysis, and Modeling in Systems Biology

“…Boolean models can predict dynamic trends in the absence of detailed kinetic parameters. For example, a Boolean gene regulatory network model of Arabidopsis floral organ development (Mendoza and Alvarez-Buylla, 1998;Espinosa-Soto et al, 2004) offered a mechanistic and dynamic explanation for the conceptual ABC model (Coen and Meyerowitz, 1991), successfully reproduced experimental gene expression patterns in wild-type and mutant plants, and predicted that cell fate determination is determined by the network architecture rather than precise interaction parameters or initial conditions. The model also proposed four novel interactions and predicts the effects of evolutionary differences in the network architecture between Arabidopsis and Petunia hybrida.…”

Schaffner's Model of Theory Reduction: Critique and Reconstruction

“…In this case, T 2 is a structured set of phenotypic characters. One example is the important ABC model of qualitative phenotype of the flowers of Arabidopsis and other plant species (e.g., Coen and Meyerowitz 1991;Espinosa-Soto, Padilla-Longoria, and Á lvarez-Buylla 2004). Second, other work on GRN abstracts explicit mathematical models of morphological and developmental phenotype (e.g., Salazar-Ciudad and Jernvall 2002;Prusinkiewicz et al 2007).…”