The tree of life of polyamine oxidases

Abstract

Polyamine oxidases (PAOs) are characterized by a broad variability in catalytic properties and subcellular localization, and impact key cellular processes in diverse organisms. In the present study, a comprehensive phylogenetic analysis was performed to understand the evolution of PAOs across the three domains of life and particularly within eukaryotes. Phylogenetic trees show that PAO-like sequences of bacteria, archaea, and eukaryotes form three distinct clades, with the exception of a few procaryotes that probably acquired a PAO gene through horizontal transfer from a eukaryotic donor. Results strongly support a common origin for archaeal PAO-like proteins and eukaryotic PAOs, as well as a shared origin between PAOs and monoamine oxidases. Within eukaryotes, four main lineages were identified that likely originated from an ancestral eukaryotic PAO before the split of the main superphyla, followed by specific gene losses in each superphylum. Plant PAOs show the highest diversity within eukaryotes and belong to three distinct clades that underwent to multiple events of gene duplication and gene loss. Peptide deletion along the evolution of plant PAOs of Clade I accounted for further diversification of function and subcellular localization. This study provides a reference for future structure-function studies and emphasizes the importance of extending comparisons among PAO subfamilies across multiple eukaryotic superphyla.

Figure 1

Maximum likelihood tree depicting the phylogenetic relationships between eukaryote PAOs and related PAO-like enzymes in bacteria and archaea; the tree is drawn to scale, with branch lengths measured in number of substitutions per site. Bootstrap support values (ultrafast bootstrap approximation) over 1000 replicates are reported in correspondence of the main nodes. The analysis involved 300 amino acidic sequences (see Supplementary Table S1). Sequences are coloured according to the three main domains of life: eukaryote = green, archaea = blue, and bacteria = red. The three main clades are named as follow: Eukaryota clade, Archaea clade, Bacteria clade; prokaryotic sequences clustering within the Eukaryota clade and non-archaean sequences clustering within the Archaea clade are indicated by black arrows.

Figure 2

Phylogeny of eukaryote PAOs based on the 253 amino acidic sequences of the Eukaryota clade of Fig. 1. The tree shown was estimated with the Maximum likelihood method under the WAG + I + G model of amino acid replacement. Nodal support (> 70) is reported along the main branches: above, ultrafast bootstrap approximation (1000 replicates); below, SH-like approximate likelihood ratio test (1000 replicates). Main clades and eukaryote groups are indicated.

Figure 3

Maximum likelihood phylogeny of plant PAOs of the ZmPAO1/AtPAO1-like clade (see Fig. 2) based on 81 amino acidic sequences. Main clades are labelled from a to f; bootstrap values of support (BS) are reported along the branches (BS > 70). Box (a) illustrates the evolutionary model for the AtPAO1-like proteins with two gene duplications (GD) in correspondence of node a and b (giving rise to the AtPAO1 subclade), and the loss of peptide A (pA) and of the signal peptide (sP) in correspondence of node f. Putative gene extinctions are indicated with ‘x’, whereas ‘?’ denote missing information on the Gymnosperm group.

Figure 4

Maximum likelihood phylogeny of plant PAOs of the AtPAO5-like clade (see Fig. 2) based on 59 amino acidic sequences. Bootstrap values of support (BS) are reported along the branches (BS > 70).

Figure 5

Maximum likelihood phylogeny of plant PAOs of the AtPAO2,3,4-like clade (see Fig. 2) based on 100 amino acidic sequences. Main clades are labelled from a to c; bootstrap values of support (BS) are reported along the branches (BS > 70). Box (a) illustrates the evolutionary model for the AtPAO2,3,4-like proteins with two gene duplications (GD) in correspondence of node a (giving rise to the AtPAO2,3 and AtAPO4 subclades) and d.