Evolutionary Dynamics of FLC-like MADS-Box Genes in Brassicaceae

Abstract

MADS-box genes encode transcription factors that play important roles in the development and evolution of plants. There are more than a dozen clades of MADS-box genes in angiosperms, of which those with functions in the specification of floral organ identity are especially well-known. From what has been elucidated in the model plant Arabidopsis thaliana, the clade of FLC-like MADS-box genes, comprising FLC-like genes sensu strictu and MAF-like genes, are somewhat special among the MADS-box genes of plants since FLC-like genes, especially MAF-like genes, show unusual evolutionary dynamics, in that they generate clusters of tandemly duplicated genes. Here, we make use of the latest genomic data of Brassicaceae to study this remarkable feature of the FLC-like genes in a phylogenetic context. We have identified all FLC-like genes in the genomes of 29 species of Brassicaceae and reconstructed the phylogeny of these genes employing a Maximum Likelihood method. In addition, we conducted selection analyses using PAML. Our results reveal that there are three major clades of FLC-like genes in Brassicaceae that all evolve under purifying selection but with remarkably different strengths. We confirm that the tandem arrangement of MAF-like genes in the genomes of Brassicaceae resulted in a high rate of duplications and losses. Interestingly, MAF-like genes also seem to be prone to transposition. Considering the role of FLC-like genes sensu lato (s.l.) in the timing of floral transition, we hypothesize that this rapid evolution of the MAF-like genes was a main contributor to the successful adaptation of Brassicaceae to different environments.

Keywords: MADS-box gene; comparative transcriptomics; phylogenomics; transcription factor.

Figure 1

Phylogeny of FLC-like genes s.l. The phylogeny was reconstructed using RaxML [50] based on a protein alignment of conceptually translated coding sequences. Numbers on the nodes represent bootstrap values. Gene names are colored according to the lineage of Brassicaceae in which they were identified. The clades are shaded: blue, MAF4/5-like genes; red, MAF1/2/3-like genes; green, FLC-like genes s.str. FLC-like genes from Tarenaya hassleriana were used as sister and outgroup representatives.

Figure 2

Phylogeny of Brassicaceae species and Tarenaya hassleriana showing events in the evolution of FLC-like genes s.l. and genomic arrangement of MAF-like genes. This phylogeny is based on the one by Walden et al., 2020 [40] and was pruned to include only the species studied here. Species names are colored according to the lineage of Brassicaceae they belong to, as explained at the top left. The numbers of identified FLC-like genes s.str. and MAF-like genes are indicated for each species in brackets after the species name. Based on the phylogeny of FLC-like genes s.l. (Figure 1), duplications, triplications, duplications involving transposition, and gene losses were inferred for FLC-like genes s.str., MAF1/2/3- and MAF4/5-like genes and are marked on the phylogeny. The meaning of the symbols is explained above the phylogeny. If there are several events on one branch, the order and the timing of these events are unknown and were chosen arbitrarily. The genomic arrangement of the MAF-like genes is shown on the right, where MAF1/2/3-like genes are indicated by red boxes and MAF4/5-like genes are shown as blue boxes. The size of the genes and the distance between the genes are not drawn to scale. Gray boxes represent incomplete genes.