Comprehensive interaction map of the Arabidopsis MADS Box transcription factors

Abstract

Interactions between proteins are essential for their functioning and the biological processes they control. The elucidation of interaction maps based on yeast studies is a first step toward the understanding of molecular networks and provides a framework of proteins that possess the capacity and specificity to interact. Here, we present a comprehensive plant protein-protein interactome map of nearly all members of the Arabidopsis thaliana MADS box transcription factor family. A matrix-based yeast two-hybrid screen of >100 members of this family revealed a collection of specific heterodimers and a few homodimers. Clustering of proteins with similar interaction patterns pinpoints proteins involved in the same developmental program and provides valuable information about the participation of uncharacterized proteins in these programs. Furthermore, a model is proposed that integrates the floral induction and floral organ formation networks based on the interactions between the proteins involved. Heterodimers between flower induction and floral organ identity proteins were observed, which point to (auto)regulatory mechanisms that prevent the activity of flower induction proteins in the flower.

Figure 1.

The Arabidopsis MADS Box Transcription Factor Interaction Matrix. The MADS box transcription factors are arranged according to their phylogenetic relationship as has been reported by Pařenicová et al. (2003). The phylogenetic trees are indicated on the x and y axis with the different groups indicated (Mα, Mβ, Mγ, Mδ, and MIKC). Protein–protein interactions are represented by red blocks, no interactions by green blocks, and interactions that could not be tested by gray blocks.

Figure 2.

Interactome Map of the Arabidopsis MADS Box Transcription Factor Family. Proteins are organized based on hierarchical clustering of their protein–protein interaction patterns. Proteins that do not interact in the screen are omitted from this figure. Protein–protein interactions are indicated with red blocks and no interactions with green blocks. Presence of clustered proteins with a putative similar function is indicated with a colored bar on the left and bottom side of the figure: red for embryo, green for root, blue for flowering, and yellow for floral organs.

Figure 3.

Subset of Arabidopsis MADS Box Transcription Factor Interactions Confirmed by Interologs. Proteins are indicated by ovals and protein interactions with lines. The color of the line corresponds with the species for which orthologous interactions have been reported (Arabidopsis [At], purple; petunia [Ph], orange; A. majus [Am], black; rice [Os], green; Gerbera hybrida [Gh], red; tobacco [Nt], blue; tomato [Le], gray; maize [Zm], yellow; lily [Ll], cyan; chrysanthemum [Cd], pink). The AP3-PI heterodimer is included in the figure because many interologs have been reported, although the full-length Arabidopsis proteins do not interact detectably in yeast. The references used to create this subset of conserved interactions are presented online (see Supplemental Table 4 online).

Figure 4.

Comparison of Expression Patterns of Genes That Encode Interacting Proteins. The data from the AtGenExpress expression atlas are represented such that expression of each gene is normalized across the entire data set. The most important groups of tissues are indicated at the top and in detail numbered in the bottom (list of all tissues is presented in Supplemental Table 5 online). Blue indicates underexpression and red overexpression relative to the mean, with yellow expression levels that are close to the average for the corresponding gene.

Figure 5.

Representation of the Flower Induction and Flower Formation Networks. Proteins are indicated by ovals (red for the flower induction, blue for the flower formation network, green for the hubs), and interactions are represented by lines. The proteins SOC1 and AGL24 form a homodimer, which is indicated with a small dot next to the oval of the protein.