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, 97 (10), 5328-33

An Ancestral MADS-box Gene Duplication Occurred Before the Divergence of Plants and Animals

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An Ancestral MADS-box Gene Duplication Occurred Before the Divergence of Plants and Animals

E R Alvarez-Buylla et al. Proc Natl Acad Sci U S A.

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. Here we suggest that a gene duplication ancestral to the divergence of plants and animals gave rise to two main lineages of MADS-box genes: TypeI and TypeII. We locate the root of the eukaryotic MADS-box gene family between these two lineages. A novel monophyletic group of plant MADS domains (AGL34 like) seems to be more closely related to previously identified animal SRF-like MADS domains to form TypeI lineage. Most other plant sequences form a clear monophyletic group with animal MEF2-like domains to form TypeII lineage. Only plant TypeII members have a K domain that is downstream of the MADS domain in most plant members previously identified. This suggests that the K domain evolved after the duplication that gave rise to the two lineages. Finally, a group of intermediate plant sequences could be the result of recombination events. These analyses may guide the search for MADS-box sequences in basal eukaryotes and the phylogenetic placement of new genes from other plant species.

Figures

Figure 1
Figure 1
Schematic representation of the protein domains of plant, animal, and fungal TypeI (SRF-like) and TypeII (MEF2-like) MADS-domain proteins. The scale indicates the number of amino acids along the protein. Plant TypeII-like proteins have carboxyl-terminal domains that go beyond 200 amino acids. In plant TypeI-like proteins the “?” indicates carboxyl-terminal domains not well defined yet and of variable lengths.
Figure 2
Figure 2
Amino acid alignment of the MADS-domain (amino acids 1 to 60) for some representative members of the plant, animal, and fungal TypeI (SRF-like) and TypeII (MEF2-like) lineages. We also show representative sequences of the genes that are not clearly assigned to either one (MADS-domains Type?). One gene from each monophyletic clade identified in MP and NJ was selected. Conserved amino acids within each group and not found in any (or in no more than two) of the MADS domains of the other group are in red. Green names indicate plant sequences and red names, animal or fungal ones (see Materials and Methods).
Figure 3
Figure 3
Phylogeny of the eukaryotic MADS-box gene family. Animal and fungal sequences (H. sapiens: MEF2A_Hs, MEF2C_Hs, MEF2D_Hs, MEF2B_Hs, SRF_Hs; X. laevis: SRF_Xl; C. elegans: CEMEF2, H. roretzi: ASMEF2; D. melanogaster: DMEF2; DSRF; S. cerevisiae: SMP1_Sc, RLM1_Sc, MCM1, ARG80; S. pombe: PLNYEAST) are red; plant sequences (all from A. thaliana) are green; bacterial USP family sequences (E. coli: EcuspA, Ecyiit; Coxiella burnetti: CoxYfmu; B. subtilis: Bsyxie) (23) are blue. TypeI (SRF-like) and TypeII (MEF2-like) lineages are indicated by blue and pink brackets, respectively. (a) The NJ tree rooted with the bacterial USP family (see ref. 23) is shown in a, and the NJ tree rooted by minimizing the reconciliation cost (see Materials and Methods) is shown in b. Branch lengths are proportional to the number of amino acid substitutions. Bootstrap values shown on branches; in b, values in parentheses correspond to analyses done without the underlined sequences. Branches with bootstrap values <50% are collapsed. Sequences within purple square are those for which a coiled-coil structure downstream of the MADS-domain (K domain) was predicted.
Figure 4
Figure 4
Model for the evolution of the MADS-box gene family in eukaryotes. At least one duplication of the ancestral MADS-box gene is postulated to have occurred before the divergence of plants and animals. The K domain was probably added to the plant TypeII (MEF2-like) lineage. Similarly, animal MADS-domain proteins evolved specific domains (SAM and MEF2) in SRF-like and MEF2-like lineages, respectively. Pink, TypeI (SRF-like) lineage; blue, TypeII (MEF2-like) lineage.

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