DNA transposons and the evolution of eukaryotic genomes

Abstract

Transposable elements are mobile genetic units that exhibit broad diversity in their structure and transposition mechanisms. Transposable elements occupy a large fraction of many eukaryotic genomes and their movement and accumulation represent a major force shaping the genes and genomes of almost all organisms. This review focuses on DNA-mediated or class 2 transposons and emphasizes how this class of elements is distinguished from other types of mobile elements in terms of their structure, amplification dynamics, and genomic effect. We provide an up-to-date outlook on the diversity and taxonomic distribution of all major types of DNA transposons in eukaryotes, including Helitrons and Mavericks. We discuss some of the evolutionary forces that influence their maintenance and diversification in various genomic environments. Finally, we highlight how the distinctive biological features of DNA transposons have contributed to shape genome architecture and led to the emergence of genetic innovations in different eukaryotic lineages.

Figure 1

Distribution of the major groups of DNA transposons across the eukaryotic tree of life. The tree depicts 4 of the 5 “supergroups” of eukaryotes (based on Keeling et al. 2005**AU: Please check: 2005 reference is listed only. 2005 is ok) where DNA transposons have been detected. The “unikonts” are represented by the opisthokonts (vertebrates, invertebrates, and fungi) and by the Ameobozoa Entamoeba, the Chromoalveolates by the oomycete Phytophtora infestans, the diatom Thalassiosira pseudonana and several ciliates, the Plantae by the unicellular green algae Chlamydomonas reinhardtii and a broad range of flowering plants, and the Excavates by the parabasalid Trichomonas vaginalis. The occurrence of each superfamily/subclass of DNA transposons is denoted by a different symbol. The data were primarily gathered from the literature (references available upon request). Open symbols denote unpublished observations gathered by the authors or from Repbase (http://www.girinst.org). The taxonomic breadth of the different groups among the 5 supergroups of eukaryotes is shown in parentheses. These data suggest that 11 of the 12 major types of DNA transposons were already diversified in the common ancestor of eukaryotes.

Figure 2

The relative amount of retrotransposons and DNA transposons in diverse eukaryotic genomes. The graph shows the contribution of DNA transposons and retrotransposons in percentage relative to the total number of transposable elements in each species. The data were compiled from papers reporting draft genome sequences (references available upon request) and from the Repeatmasker output tables available at the UCSC Genome Browser (http://genome.ucsc.edu) or from the following sources: E. histolytica and E. invadens: (159); T. vaginalis: E. Pritham, unpublished data. Species abbreviations: Sc: Saccharomyces cerevisiae; Sp: Schizosaccharomyces pombe; Hs: Homo sapiens; Mm: Mus musculus; Os: Oryza sativa; Ce: Caenorhabditis elegans; Dm: Drosophila melanogaster; Ag: Anopheles gambiae, malaria mosquito; Aa: Aedes aegypti, yellow fever mosquito; Eh: Entamoeba histolytica; Ei: Entamoeba invadens; Tv: Trichomonas vaginalis.

Figure 3. Model for the assembly of a regulatory network by domestication of a transposase and its binding sites

A: Initial transposase domestication event. A family of DNA transposon is shown with autonomous and nonautonomous copies dispersed in the genome. Each TIR (black arrowhead) contains a binding site for a transposase encoded by autonomous copies (pink/yellow boxes). Flanking host genes are shown as grey boxes. One of the transposase genes (yellow box) is recruited. In this example, recruitment is promoted by transcriptional fusion of the transposase to a flanking host gene (blue box) encoding a regulatory domain, leading to the expression of a fusion protein with transpoase (yellow) and regulatory domains (blue). This is similar to the emergence of SETMAR, which arose by fusion of a mariner transposase with an adjacent gene encoding a SET domain. Note however that transposase domestication does not need to involve fusion with another domain, particularly if the transposase itself possesses regulatory activity, as demonstrated for FHY3, a transcription factor in Arabidopsis entirely derived from a Mutator transposase. B: Immediate consequences of transposase domestication. The translational fusion immediately allows the regulatory domain to be tethered to all the sites in the genome recognized by the transposase, i.e. the TIRs of all the transposon copies previously dispersed in the genome. Depending on the genomic environment of the transposons, binding of the fusion protein might have various effects on the expression of the surrounding genes: activation, repression or no effect. These effects are symbolized by the blue arrow acting on adjacent gene. C: Binding sites selection. Natural selection will retain interactions that provide an immediate benefit to the host and will eliminate deleterious interactions. Site elimination (red cross) may occur through substitutions or deletion driven by positive selection. Sites that are selectively neutral (with no positive or negative impact on adjacent genes) are expected to evolve neutrally and most will eventually disappear. Mobility of the transposons at this stage (if it persists) might accelerate the shaping of the network through transposon excision events and/or fixation of new advantageous insertions. D: A regulatory network is born. The end result is the assembly of a regulatory network, where the domesticated transposase and a subset of its ancestral binding sites conferring beneficial interactions are evolving under purifying selection, while the rest of the transposons are eroded by mutations. Note that the system also provides an intuitive opportunity for the establishment of a feedback loop “F” (positive or negative) through domestication of binding sites that were originally linked to the domesticated transposase.