Abstract
DEF-like and GLO-like class B floral homeotic genes encode closely related MADS-domain transcription factors that act as developmental switches involved in specifying the identity of petals and stamens during flower development. Class B gene function requires transcriptional upregulation by an autoregulatory loop that depends on obligate heterodimerization of DEF-like and GLO-like proteins. Because switch-like behavior of gene expression can be displayed by single genes already, the functional relevance of this complex circuitry has remained enigmatic. On the basis of a stochastic in silico model of class B gene and protein interactions, we suggest that obligate heterodimerization of class B floral homeotic proteins is not simply the result of neutral drift but enhanced the robustness of cell-fate organ identity decisions in the presence of stochastic noise. This finding strongly corroborates the view that the appearance of this regulatory mechanism during angiosperm phylogeny led to a canalization of flower development and evolution.
Highlights
Depending on the nature of the interactions of their constituents, gene regulatory circuits can display a variety of dynamical behaviors ranging from simple steady states, to switching and multistability, to oscillations
Our results suggest that identifying these different induction pathways, and clarifying their molecular mechanisms would enable an important step forward in understanding class B floral homeotic gene function in flowering plants
Given that the duplicates resulting from one homodimerizing protein would be capable of homo- as well as heterodimerization, our results suggest that positive selection should have enforced the loss of the homodimerization ability, since our model with duplicated class B genes and obligatory heterodimerization implies a sharper switching characteristic and a more constrained domain of class B gene expression than the one with facultative heterodimerization
Summary
Depending on the nature of the interactions of their constituents, gene regulatory circuits can display a variety of dynamical behaviors ranging from simple steady states, to switching and multistability, to oscillations. Comparing one autoregulatory class B gene with the circuit after duplication and reduction to obligate heterodimerization, our model suggests that an important difference lies in the response to larger numbers of activatory molecules, where the latter system exhibits a clearly reduced tendency to switch off by mistake This is explained by the fact that the circuit needs both DEF-like and GLO-like proteins to sustain activation, its two pools of gene products provide a buffer to temporary stochastic failure of one of the two genes. Our results suggest that identifying these different induction pathways, and clarifying their molecular mechanisms (e.g., trans-acting factors and cis-regulatory DNA motifs in DEF-like and GLO-like genes being involved) would enable an important step forward in understanding class B floral homeotic gene function in flowering plants. This underlines the hypothesis [25] that the mechanism described here improves developmental robustness and helped to canalize the development and the evolution of flowers within angiosperm evolution
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