A hitchhiker's guide to the MADS world of plants

Abstract

Plant life critically depends on the function of MADS-box genes encoding MADS-domain transcription factors, which are present to a limited extent in nearly all major eukaryotic groups, but constitute a large gene family in land plants. There are two types of MADS-box genes, termed type I and type II, and in plants these groups are distinguished by exon-intron and domain structure, rates of evolution, developmental function and degree of functional redundancy. The type I genes are further subdivided into three groups - M alpha, M beta and M gamma - while the type II genes are subdivided into the MIKCC and MIKC* groups. The functional diversification of MIKCC genes is closely linked to the origin of developmental and morphological novelties in the sporophytic (usually diploid) generation of seed plants, most spectacularly the floral organs and fruits of angiosperms. Functional studies suggest different specializations for the different classes of genes; whereas type I genes may preferentially contribute to female gametophyte, embryo and seed development and MIKC*-group genes to male gametophyte development, the MIKCC-group genes became essential for diverse aspects of sporophyte development. Beyond the usual transcriptional regulation, including feedback and feed-forward loops, various specialized mechanisms have evolved to control the expression of MADS-box genes, such as epigenetic control and regulation by small RNAs. In future, more data from genome projects and reverse genetic studies will allow us to understand the birth, functional diversification and death of members of this dynamic and important family of transcription factors in much more detail.

Figure 1

Primary and domain structure of MADS-domain proteins. (a) Sequence logo of the MADS domain based on 6,668 sequences belonging to the MADS superfamily (accession number cl00109) as defined by the Conserved Domains Database at the National Center for Biotechnology Information [65]. Sequences were aligned using hmmalign of the HMMer package [66] and the logo was created using WebLogo [67]. The logo displays the frequencies of amino acids at each position of the MADS domain, as the relative heights of letters, along with the degree of conservation as the total height of a stack of letters, measured in bits of information. The conserved motif KR[K/R]X₄KK, which serves as part of the nuclear localization signal, is indicated by a black line. (b) Domain structure of MADS domain proteins in plants. Type I proteins do not have distinct conserved domains other than the SRF-like MADS domain whereas the MEF2-like MADS domain of type II (MIKC-type) proteins of plants is followed by the intervening (I), the keratin-like (K) and the C-terminal (C) domains. Orange indicates a role in DNA binding, blue denotes a role in protein-protein interaction, and purple indicates a role in transactivation. The three subdomains of the K domain, K1, K2 and K3, are indicated by black lines.

Figure 2

Phylogeny of representative plant species, including some for which the whole genome has been sequenced and some species for which whole-genome information is not available (shaded names). The number of known type I (red), MIKC^C-group (green) and MIKC*-group (blue) MADS-box genes for extant plant species and the estimated minimal number of MADS-box genes for ancestral plant species are indicated on the corresponding branches. Numbers in yellow boxes indicate the number of MIKC-type genes that have not diverged into MIKC^C- or MIKC*-group genes. The '?' indicates that no information on the number of the respective type or group of MADS-box genes is available. The red arrow denotes the time when the K domain joined a type II MADS domain, and the black arrow indicates the divergence of an ancestral MIKC-type MADS-box gene into MIKC^C- and MIKC*-group genes. MYA, million years ago.

Figure 3

Phylogenies of representative type I and type II MADS-box genes from different, distantly related plant species. (a) type I; (b) type II. Phylogenies were determined using MrBayes [68] on protein-guided nucleotide alignments, using the type I MADS-box gene of O. lucimarinus (PrID 120540) and the type II MADS-box gene CgMADS1 of Chara globularis as representatives of the outgroup, respectively, and creating 3,000,000 generations. Genes from monocots (gray) and eudicots (green) are shaded. Different groups and/or clades of MADS-box genes are colored differently. GGM13 (Bsister), Gnetum gnemon MADS13; SQUA, SQUAMOSA; STMADS11, Solanum tuberosum MADS11; TM3, tomato MADS3; GLO, GLOBOSA; other abbreviations are defined in the text and Table 1.

Figure 4

Structures of MADS-domain proteins and their functions in determining floral identity. (a) Crystal structure of a dimer of the MADS-domain of human serum response factor (SRF) bound to DNA (PDB 1SRS; note that no crystal structure exists for plant MADS-domain proteins). DNA is shown in ball-and-stick representation and colored in gray, while the two MADS domains of the dimer are colored blue and red, respectively. The α-helix is represented by a spring-like structure whereas the β-strands are shown as darker colored arrows. (b) Structures of 'floral quartets'. According to the floral quartet model, multimeric complexes of MIKC^C-group proteins, bound to two DNA sequence elements (CArG-boxes) present in numerous target genes, determine floral organ identity. Specifically, quartet formation involving two dimers of AG and SEP proteins (Table 1) determines carpel identity; complex formation involving a dimer of AG and SEP with a dimer of AP3 and PI determines stamen identity; quartet formation involving a dimer of AP1 and SEP with a dimer of AP3 and PI determines petal identity; and complex formation involving two dimers of AP1 and SEP determines sepal identity. CArG1-3, different CArG-boxes.

Figure 5

Different phases of the flowering-plant life cycle are controlled preferentially by different classes of MADS-box genes. While most phases of the development of the diploid sporophyte involve MIKC^C-group gene action (green), male gametophyte (pollen) development is dominated by the activity of MIKC*-group genes (blue) and the development of the female gametophyte (embryo sac), embryo and seed is mainly controlled by type I genes (pink).