An ancestral MADS-box gene duplication occurred before the divergence of plants and animals

Abstract

Changes in genes encoding transcriptional regulators can alter development and are important components of the molecular mechanisms of morphological evolution. MADS-box genes encode transcriptional regulators of diverse and important biological functions. In plants, MADS-box genes regulate flower, fruit, leaf, and root development. Recent sequencing efforts in Arabidopsis have allowed a nearly complete sampling of the MADS-box gene family from a single plant, something that was lacking in previous phylogenetic studies. To test the long-suspected parallel between the evolution of the MADS-box gene family and the evolution of plant form, a polarized gene phylogeny is necessary. MEF2 ͉ SRF ͉ homeotic genes ͉ MADS ͉ development C hanges in genes encoding transcriptional regulators may represent the most important determinants of morphological evolution in plants and animals (1), and phylogenetic analyses provide a historical framework to identify such changes. The MADS-box genes encode a eukaryotic family of transcriptional regulators involved in diverse and important biological functions, ranging from cardiac muscle development in animals to pheromone response in yeast (2). In plants, MADS-box genes encode the three floral homeotic functions predicted by the genetic ABC model of flower organ identity (3, 4). In addition, plant MADS-box genes regulate the timing of flower initiation and flower meristem identity, as well as various aspects of ovule, fruit, leaf, and root development (4, 5).Previously identified plant MADS-box genes encode proteins that share a stereotypical MIKC structure (Fig. 1), with the highly conserved DNA-binding MADS domain at the amino terminus. The moderately conserved K domain in the central portion of these proteins has been shown to be important for protein-protein interactions and likely forms a coiled-coil structure. The MADS and K domains are linked to one another by a weakly conserved I domain, whereas a poorly conserved carboxyl-terminal (C) region may function as a trans-activation domain (4). In animals and fungi, two distinct types of MADSbox genes have been identified, the SRF-like and MEF2-like classes (ref. 2; see Fig. 1).This paper provides a hypothesis on the evolutionary history of the eukaryotic MADS-box gene family. Previous studies of eukaryotic MADS-box gene evolution, which included plant and animal sequences, provided unrooted trees useful to infer the phylogenetic relationships of the MADS-box lineages (6). These previous studies suggested that at least one MADS-box gene was present in the common ancestor of plants, animals, and fungi, and that probably the duplication that gave rise to the animal MEF2-and SRF-like genes occurred after animals diverged from plants but before fungi diverged from animals (6). However, previous plant and eukaryotic studies were based on a relatively small sampling of plant MADS-box sequences for a particular species (6-9). To test whether all Arabidopsis MADSbox sequences group in a monophyletic clade distinct from all animal and fungal ...

APETALA1 and SEPALLATA3 interact to promote flower development

“…Of the clones from this screen, one started in the MADS box and three began in the I region. SVP was identi®ed as an Arabidopsisexpressed sequence tag with homology to the MADS-box family (Alvarez-Buylla et al, 2000a), and was also cloned by Hartman et al (2000) through transposon tagging. SVP is a repressor of¯owering and is expressed in young leaves and throughout the shoot apical meristem during vegetative development.…”

“…In addition, recent studies have shown that a trio of closely related genes, SEPALLATA1/2/3 (SEP1/ 2/3), are required for petal, stamen and carpel identity, and are thus necessary for the activities of the B-and Cfunction genes (Pelaz et al, 2000). Remarkably, with the exception of the AP2 gene, all the other organ-identity genes belong to the extended family of MADS-box genes, a family that is known to include more than 44 distinct sequences in Arabidopsis (Alvarez- Buylla et al, 2000a;Davies and Schwarz-Sommer, 1994;Purugganan et al, 1995;Rounsley et al, 1995). MADS-domain proteins, well characterized in yeast (MCM1, Ammererer, 1990) and mammals (SRF, Norman et al, 1988), form dimers that bind to DNA and form ternary complexes with many unrelated proteins (Lamb and McKnight, 1991;Shore and Sharrocks, 1995).…”

Selection on Length Mutations After Frameshift Can Explain the Origin and Retention of the AP3/DEF-Like Paralogues in Impatiens

“…Floral homeotic class B genes, which comprise AP3/DEF and PI/GLO, are required for petal identity in the second whorl and stamen identity in the third whorl of eudicot flowers (Jack et al 1992(Jack et al , 1994Goto and Meyerowitz 1994;Theissen et al 2000;Alvarez-Buylla et al 2000). AP3/DEF belong to the type II class MADSbox genes, consisting of four distinct regions: a MADS domain (M), an intervening region (I), a keratine-like domain (K), and a C-terminus (C) (Munster et al 1997).…”

The K domain mediates heterodimerization of theArabidopsisfloral organ identity proteins, APETALA3 and PISTILLATA

“…MADS genes in Arabidopsis function to regulate diverse developmental events such as flowering time control, meristem identity, floral organ development and fruit development (Alvarez-Buylla et al, 2000b;Initiative, 2000;Riechmann et al, 2000;Theißen et al, 2000). MADS proteins function as dimeric DNA-binding proteins.…”