Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny

Abstract

Gene duplication is a substrate of evolution. However, the relative importance of positive selection versus relaxation of constraints in the functional divergence of gene copies is still under debate. Plant MADS-box genes encode transcriptional regulators key in various aspects of development and have undergone extensive duplications to form a large family. We recovered 104 MADS sequences from the Arabidopsis genome. Bayesian phylogenetic trees recover type II lineage as a monophyletic group and resolve a branching sequence of monophyletic groups within this lineage. The type I lineage is comprised of several divergent groups. However, contrasting gene structure and patterns of chromosomal distribution between type I and II sequences suggest that they had different evolutionary histories and support the placement of the root of the gene family between these two groups. Site-specific and site-branch analyses of positive Darwinian selection (PDS) suggest that different selection regimes could have affected the evolution of these lineages. We found evidence for PDS along the branch leading to flowering time genes that have a direct impact on plant fitness. Sites with high probabilities of having been under PDS were found in the MADS and K domains, suggesting that these played important roles in the acquisition of novel functions during MADS-box diversification. Detected sites are targets for further experimental analyses. We argue that adaptive changes in MADS-domain protein sequences have been important for their functional divergence, suggesting that changes within coding regions of transcriptional regulators have influenced phenotypic evolution of plants.

Fig. 1.

A. thaliana MADS-box gene family Bayesian phylogeny. Numbers above or below branches represent Bayesian posterior probabilities of finding a given clade. Branch lengths are proportional to number of nucleotide substitutions. AGL105 was excluded.

Fig. 2.

Type I and type II A. thaliana MADS-box Bayesian phylogenies. (a) Type I tree polarized with type II sequences. (b) Type II tree polarized with type I sequences. Numbers above or below branches represent posterior probabilities. Branch lengths are proportional to the number of nucleotide substitutions. Boxed letters identify clades in which site-specific tests of positive selection yielded statistically significant LRT results for at least two model comparisons and in which at least one of the models detected sites under PDS with PP > 0.90. Branches underlined with a broken line identify cases in which the branch-site analyses yielded significant PDS results. #, Excluded from the site-specific analyses.

Fig. 3.

Schematic representation of the distribution of sites under PDS in type I (a) and type II (b) sequences. MADS, I, K, and COOH domains are indicated. In a, the upper row corresponds to branch-site analysis along the branch leading to PHERES1, and the rest of the rows correspond, from top to bottom, to the site analyses performed below the nodes marked with the boxed letters AG, AH, AL, AP, AQ, and AR in Fig. 2a. In b, the upper row corresponds to branch-site analysis along the FLC branch and the lower row corresponds to branch-site analysis along the SVP branch. In a, the upper scale corresponds to amino acid position along the MADS domain and the lower scale corresponds to amino acid position along our alignment. In b, the scale corresponds to amino acid position along our alignment. Sites with PP > 0.70 are included. Shaded regions in b were excluded from PDS to avoid false positives. All sites are listed in Tables 1 and 2.