Combining Phylogenetic and Syntenic Analyses for Understanding the Evolution of TCP ECE Genes in Eudicots

Abstract

TCP ECE genes encode transcription factors which have received much attention for their repeated recruitment in the control of floral symmetry in core eudicots, and more recently in monocots. Major duplications of TCP ECE genes have been described in core eudicots, but the evolutionary history of this gene family is unknown in basal eudicots. Reconstructing the phylogeny of ECE genes in basal eudicots will help set a framework for understanding the functional evolution of these genes. TCP ECE genes were sequenced in all major lineages of basal eudicots and Gunnera which belongs to the sister clade to all other core eudicots. We show that in these lineages they have a complex evolutionary history with repeated duplications. We estimate the timing of the two major duplications already identified in the core eudicots within a timeframe before the divergence of Gunnera and after the divergence of Proteales. We also use a synteny-based approach to examine the extent to which the expansion of TCP ECE genes in diverse eudicot lineages may be due to genome-wide duplications. The three major core-eudicot specific clades share a number of collinear genes, and their common evolutionary history may have originated at the γ event. Genomic comparisons in Arabidopsis thaliana and Solanum lycopersicum highlight their separate polyploid origin, with syntenic fragments with and without TCP ECE genes showing differential gene loss and genomic rearrangements. Comparison between recently available genomes from two basal eudicots Aquilegia coerulea and Nelumbo nucifera suggests that the two TCP ECE paralogs in these species are also derived from large-scale duplications. TCP ECE loci from basal eudicots share many features with the three main core eudicot loci, and allow us to infer the makeup of the ancestral eudicot locus.

Evolution and Expression Patterns of TCP Genes in Asparagales

“…Our analysis also recovers the previously identified duplication of CYC-like genes in basal eudicots (Citerne et al, 2013), and another in Poales, the latter resulting in the REP1/TB1 clades (Mondragón-Palomino and Trontin, 2011). Most basal angiosperms and many monocots outside Poales have single copy CYC-like genes that predate the independent duplications in eudicots and Poales (Figure 1).…”

Specific Duplication and Dorsoventrally Asymmetric Expression Patterns of Cycloidea-Like Genes in Zygomorphic Species of Ranunculaceae

“…Studies in Poaceae, Zingiberales and Commelinales also suggest a possible role of T b 1-like genes, the closest C yc paralog in monocots, in the independent evolution of floral bilateral symmetry [16], [23], [24]. In parallel with the situation observed in core eudicots and monocots, independent duplications of C yc -like genes have been observed in all major lineages of basal eudicots, including the Ranunculales [25]. Studies in Fumarioideae (Papaveraceae) species showed that late expression of the two C yc -like genes was correlated with symmetry type [26], [27].…”

Analysis of the CYC/TB1 class of TCP transcription factors in basal angiosperms and magnoliids

“…The phylogenetic analysis with all newly isolated CYCL genes recovers, although with low support, the three core eudicot subclades CYC1 ( TCP18 ), CYC2 ( TCP1 ) and CYC3 ( TCP12 ), that have been previously reported (Howarth and Donoghue, ; Citerne et al ., ), likely resulting from two consecutive duplications coincident with whole genome duplications known to have occurred with the diversification of the core eudicots (Jiao et al ., ). Relationships between the subclades are unclear as there is not sufficient resolution in these nodes (Figure S1).…”