Conservation and divergence in the AGAMOUS subfamily of MADS‐box genes: evidence of independent sub‐ and neofunctionalization events

Abstract

The MADS-box gene AGAMOUS (AG) plays a key role in determining floral meristem and organ identities. We identified three AG homologs, EScaAG1, EScaAG2, and EScaAGL11 from the basal eudicot Eschscholzia californica (California poppy). Phylogenetic analyses indicate that EScaAG1 and EScaAG2 are recent paralogs within the AG clade, independent of the duplication in ancestral core eudicots that gave rise to the euAG and PLENA (PLE) orthologs. EScaAGL11 is basal to core eudicot AGL11 orthologs in a clade representing an older duplication event after the divergence of the angiosperm and gymnosperm lineages. Detailed in situ hybridization experiments show that expression of EScaAG1 and EScaAG2 is similar to AG; however, both genes appear to be expressed earlier in floral development than described in the core eudicots. A thorough examination of available expression and functional data in a phylogenetic context for members of the AG and AGL11 clades reveals that gene expression has been quite variable throughout the evolutionary history of the AG subfamily and that ovule-specific expression might have evolved more than twice. Although sub- and neofunctionalization are inferred to have occurred following gene duplication, functional divergence among orthologs is evident, as is convergence, among paralogs sampled from different species. We propose that retention of multiple AG homologs in several paralogous lineages can be explained by the conservation of ancestral protein activity combined with evolutionarily labile regulation of expression in the AG and AGL11 clades such that the collective functions of the AG subfamily in stamen and carpel development are maintained following gene duplication.

Redefining C and D in the Petunia ABC

“…A duplication event in the AG lineage at the base of the angiosperm radiation has led to the presence of two or more AG clade genes in most higher eudicot species (Kramer et al, 2004;Zahn et al, 2006). Here, we show that the petunia C-function is encoded by two genes, PMADS3 and FBP6, in a largely redundant fashion: We observed only mild phenotypes in the single loss-of-function lines, but fbp6 PMADS3-RNAi plants display a complete loss of reproductive organ identity and of determinacy.…”

“…The C-and D-lineage genes together compose the AGAMOUS (AG) subfamily within the MADS box transcription factor family. This subfamily can be divided into two clades: the C-clade (which is further divided into two subclades; the euAG-and the PLENA-subclade) and the D-clade (Colombo et al, 1995;Kramer et al, 2004;Zahn et al, 2006).…”

Functional Analysis of All AGAMOUS Subfamily Members in Rice Reveals Their Roles in Reproductive Organ Identity Determination and Meristem Determinacy

“…MADS3 and MADS58 fall into the AG lineage, whereas MADS13 and MADS21 are AGL11 lineage genes (Kramer et al, 2004;Yamaguchi et al, 2006;Dreni et al, 2007). Although Zahn et al (2006) placed MADS13 in the AG lineage, other phylogenetic analyses, gene structure, and specific amino acid residues strongly suggest that MADS13 belongs to the AGL11 lineage (Kramer et al, 2004;Dreni et al, 2007).…”

“…In Arabidopsis, four genes, AG, SHATTERPROOF1 (SHP1), SHP2, and SEEDSTICK (STK; previously known as AGL11), form the AG monophyletic subfamily within the MADS box gene phylogeny (Parenicová et al, 2003;Kramer et al, 2004;Zahn et al, 2006). Analysis of the evolutionary history of gene duplications showed that the SHP1 and SHP2 genes are the products of a recent duplication event, which probably occurred after the divergence of rosid and asterid eudicots (Vision et al, 2000).…”

“…The duplication event that gave rise to the AG (euAG clade) and the SHP genes (PLENA clade) took place early in the history of the core eudicots (Kramer et al, 2004;Zahn et al, 2006), whereas a more ancient duplication event occurred early in angiosperm evolution, marking the origin of the AG and AGL11 lineages (Kramer et al, 2004;Zahn et al, 2006).…”