Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements

Abstract

Background: Tc1/mariner transposons are widespread DNA transposable elements (TEs) that have made important contributions to the evolution of host genomic complexity in metazoans. However, the evolution and diversity of the Tc1/mariner superfamily remains poorly understood. Following recent developments in genome sequencing and the availability of a wealth of new genomes, Tc1/mariner TEs have been identified in many new taxa across the eukaryotic tree of life. To date, the majority of studies focussing on Tc1/mariner elements have considered only a single host lineage or just a small number of host lineages. Thus, much remains to be learnt about the evolution of Tc1/mariner TEs by performing analyses that consider elements that originate from across host diversity.

Results: We mined the non-redundant database of NCBI using BLASTp searches, with transposase sequences from a diverse set of reference Tc1/mariner elements as queries. A total of 5158 Tc1/mariner elements were retrieved and used to reconstruct evolutionary relationships within the superfamily. The resulting phylogeny is well resolved and includes several new groups of Tc1/mariner elements. In particular, we identify a new family of plant-genome restricted Tc1/mariner elements, which we call PlantMar. We also show that the pogo family is much larger and more diverse than previously appreciated, and we review evidence for a potential revision of its status to become a separate superfamily.

Conclusions: Our study provides an overview of Tc1-mariner phylogeny and summarises the impressive diversity of Tc1-mariner TEs among sequenced eukaryotes. Tc1/mariner TEs are successful in a wide range of eukaryotes, especially unikonts (the taxonomic supergroup containing Amoebozoa, Opisthokonta, Breviatea, and Apusomonadida). In particular, ecdysozoa, and especially arthropods, emerge as important hosts for Tc1/mariner elements (except the PlantMar family). Meanwhile, the pogo family, which is by far the largest Tc1/mariner family, also includes many elements from fungal and chordate genomes. Moreover, there is evidence of the repeated exaptation of pogo elements in vertebrates, including humans, in addition to the well-known example of CENP-B. Collectively, our findings provide a considerable advancement in understanding of Tc1/mariner elements, and more generally they suggest that much work remains to improve understanding of the diversity and evolution of DNA TEs.

Keywords: DNA transposon; Evolution; Phylogeny; Tigger; Transposable element; Transposase.

Fig. 1

Schematic providing a summary of host associations for monophyletic Tc1/mariner groups identified during phylogenetic analysis, which are illustrated as collapsed clades. For each clade (except groups containing less than 3 sequences), a schematic summarising the structure of the TEs contained within each group is illustrated, with structural features represented by different coloured rectangles (please see the accompanying key). TIR: terminal inverted repeat, ORF: open reading frame; Znf: zinc finger domain. For the Tc1, PlantMar, mariner and pogo families, pie charts show the proportion of elements extracted from each eukaryote host group. The four minor families Tec, HvSm, DD37E(L31) and TBE do not have pie charts as the number of sequences is very small

Fig. 2

Tanglegram summarising the fit between Tc1/mariner phylogeny (on the left) and eukaryotic host phylogeny (on the right). Coloured silhouettes indicate the host group that corresponds to each branch of eukaryotic diversity, and lines of corresponding colour link each TE with its host group. Where a great number of elements link to a certain host group, the lines appear as a solid block