Evolution of 14-3-3 Proteins in Angiosperm Plants: Recurring Gene Duplication and Loss

Abstract

14-3-3 proteins are key regulatory factors in plants and are involved in a broad range of physiological processes. We addressed the evolutionary history of 14-3-3s from 46 angiosperm species, including basal angiosperm Amborella and major lineage of monocotyledons and eudicotyledons. Orthologs of Arabidopsis isoforms were detected. There were several rounds of duplication events in the evolutionary history of the 14-3-3 protein family in plants. At least four subfamilies (iota, epsilon, kappa, and psi) formed as a result of ancient duplication in a common ancestor of angiosperm plants. Recent duplication events followed by gene loss in plant lineage, among others Brassicaceae, Fabaceae, and Poaceae, further shaped the high diversity of 14-3-3 isoforms in plants. Coexpression data showed that 14-3-3 proteins formed different functional groups in different species. In some species, evolutionarily related groups of 14-3-3 proteins had coexpressed together under certain physiological conditions, whereas in other species, closely related isoforms expressed in the opposite manner. A possible explanation is that gene duplication and loss is accompanied by functional plasticity of 14-3-3 proteins.

Keywords: 14-3-3 proteins; MrBayes; coexpression; gene family; molecular phylogeny; whole-genome duplication.

Figure 1

Phylogenetic tree (cladogram) of plant 14-3-3 proteins family based on Bayesian analysis of coding nucleotide sequences. Branches are coloured according to Bayesian support values, maximal support is red, minimal support is blue. Section colours indicate subfamilies. Text colours indicate epsilon (red) and non-epsilon (blue) types of isoforms. Tips of branches are omitted. Full phylogenetic tree in high resolution with all analysed 14-3-3 proteins names is presented in Supplementary (Figure S1).

Figure 2

Arabidopsis-based hierarchic classification of plant 14-3-3 proteins subfamilies. All plant 14-3-3s subdivided into two types of isoforms: epsilon and non-epsilon. At the next level of hierarchy there are six subfamilies: iota, mu, epsilon, omega, psi and kappa. In Arabidopsis, most of subfamilies include several isoforms, named by Greek letters or GRFs (General Regulatory Factors).

Figure 3

Arabidopsis thaliana 14-3-3 isoforms: phylogenetic relationships (upper graph) and coexpression under different physiological conditions (correlation heatmaps). Upper graph is unrooted NJ tree of 14-3-3s from A. thaliana, bar is number of nucleotide changes per site. Colour of a branch reflects different subfamilies groups. Correlation heatmaps show PCCs between each pair of 14-3-3s. Positive correlations are displayed in red, negative correlations are displayed in blue. The size of the circle and the colour intensity are proportional to the PCCs.

Figure 4

14-3-3 isoforms of four species: Glycine max (soybean), Medicago truncatula (barrel medic), Solanum lycopersicum (tomato) and Zea mays (maize): phylogenetic relationships (left graph) and coexpression under abiotic and biotic stress. Left graph is unrooted NJ tree of 14-3-3s, bar is number of nucleotide changes per site. Colour of a branch reflects different subfamilies groups. Correlation heatmaps show PCCs between each pair of 14-3-3s. Positive correlations are displayed in red, negative correlations are displayed in blue. The size of the circle and the colour intensity are proportional to the PCCs.

Figure 5

Oryza sativa 14-3-3 isoforms: phylogenetic relationships (upper graph) and coexpression under different physiological conditions (four correlation heatmaps). Upper graph is unrooted NJ tree of 14-3-3s from O. sativa, bar is number of nucleotide changes per site. Colour of a branch reflects different subfamilies groups. Correlation heatmaps show PCCs between each pair of 14-3-3s. Positive correlations are displayed in red, negative correlations are displayed in blue. The size of the circle and the colour intensity are proportional to the PCCs.