MADS-box transcription factors are key regulators of several plant development processes. Analysis of the complete Arabidopsis genome sequence revealed 107 genes encoding MADS-box proteins, of which 84% are of unknown function. Here, we provide a complete overview of this family, describing the gene structure, gene expression, genome localization, protein motif organization, and phylogenetic relationship of each member. We have divided this transcription factor family into five groups (named MIKC, M ␣ , M ␤ , M ␥ , and M ␦ ) based on the phylogenetic relationships of the conserved MADS-box domain. This study provides a solid base for functional genomics studies into this important family of plant regulatory genes, including the poorly characterized group of M-type MADS-box proteins. MADS-box genes also constitute an excellent system with which to study the evolution of complex gene families in higher plants.

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.

Tables S1 to S3, S5, S6, and S9 as zipped Excel files

SummaryMembers of the MADS-box transcription factor family play essential roles in almost every developmental process in plants. Many MADS-box genes have conserved functions across the flowering plants, but some have acquired novel functions in specific species during evolution. The analyses of MADS-domain protein interactions and target genes have provided new insights into their molecular functions. Here, we review recent findings on MADS-box gene functions in Arabidopsis and discuss the evolutionary history and functional diversification of this gene family in plants. We also discuss possible mechanisms of action of MADS-domain proteins based on their interactions with chromatin-associated factors and other transcriptional regulators. Key words: MADS-box genes, Plant development, Evolution, Transcriptional regulationIntroduction MADS-domain transcription factors comprise one of the beststudied gene families in plants and members of this family play prominent roles in plant development. Two decades ago, the first MADS-box genes AGAMOUS (AG) from Arabidopsis thaliana (Yanofsky et al., 1990) and DEFICIENS (DEF) from Antirrhinum majus (Schwarz-Sommer et al., 1990) were discovered as regulators of floral organ identity. The sequence of the ~60 amino acid DNA-binding domains within these proteins showed striking similarities to that of the previously characterized proteins serum response factor (SRF) in Homo sapiens (Norman et al., 1988) and Minichromosome maintenance 1 (Mcm1) in Saccharomyces cerevisiae (Passmore et al., 1988). This shared and conserved domain was named the MADS domain (for MCM1, AG, DEF and SRF) and is present in all MADS-domain transcription factor family members (Schwarz-Sommer et al., 1990). Structural analysis of animal and yeast MADS domains showed that the N-terminal and central parts of the MADS domain make contacts with the DNA, while the C-terminal part of this domain contributes mainly to protein dimerization, resulting in a DNA-binding protein dimer consisting of two interacting MADS monomers (e.g. Pellegrini et al., 1995;Huang et al., 2000). Over the past 22 years, many MADS-box gene functions were uncovered in the model species Arabidopsis thaliana and in other flowering plants. Important model plant species for MADS-box gene research include snapdragon (Antirrhinum majus) (reviewed by Schwarz-Sommer et al., 2003), tomato (Solanum lycopersicum), petunia (Petunia hybrida) (Gerats and Vandenbussche, 2005), gerbera (Gerbera hybrida) (Teeri et al., 2006) and rice (Oryza sativa) (reviewed by Yoshida and Nagato, 2011).Initially, MADS-box genes were found to be major players in floral organ specification, but more recent studies revealed functions for MADS-box genes in the morphogenesis of almost all organs and throughout the plant life cycle, from embryo to gametophyte development. The MADS-box gene family in higher plants is significantly larger than that found in animals or fungi, with more than 100 genes in representative flowering plant Development 139, 3081-3098 (2012) REVIEW Box 1...

The appropriate timing of flowering is crucial for plant reproductive success. It is therefore not surprising that intricate genetic networks have evolved to perceive and integrate both endogenous and environmental signals, such as carbohydrate and hormonal status, photoperiod and temperature. In contrast to our detailed understanding of the vernalization pathway, little is known about how flowering time is controlled in response to changes in the ambient growth temperature. In Arabidopsis thaliana, the MADS-box transcription factor genes FLOWERING LOCUS M (FLM) and SHORT VEGETATIVE PHASE (SVP) have key roles in this process. FLM is subject to temperature-dependent alternative splicing. Here we report that the two main FLM protein splice variants, FLM-β and FLM-δ, compete for interaction with the floral repressor SVP. The SVP-FLM-β complex is predominately formed at low temperatures and prevents precocious flowering. By contrast, the competing SVP-FLM-δ complex is impaired in DNA binding and acts as a dominant-negative activator of flowering at higher temperatures. Our results show a new mechanism that controls the timing of the floral transition in response to changes in ambient temperature. A better understanding of how temperature controls the molecular mechanisms of flowering will be important to cope with current changes in global climate.