Mammalian transposable elements and their impacts on genome evolution

Abstract

Transposable elements (TEs) are genetic elements with the ability to mobilize and replicate themselves in a genome. Mammalian genomes are dominated by TEs, which can reach copy numbers in the hundreds of thousands. As a result, TEs have had significant impacts on mammalian evolution. Here we summarize the current understanding of TE content in mammal genomes and find that, with a few exceptions, most fall within a predictable range of observations. First, one third to one half of the genome is derived from TEs. Second, most mammalian genomes are dominated by LINE and SINE retrotransposons, more limited LTR retrotransposons, and minimal DNA transposon accumulation. Third, most mammal genome contains at least one family of actively accumulating retrotransposon. Finally, horizontal transfer of TEs among lineages is rare. TE exaptation events are being recognized with increasing frequency. Despite these beneficial aspects of TE content and activity, the majority of TE insertions are neutral or deleterious. To limit the deleterious effects of TE proliferation, the genome has evolved several defense mechanisms that act at the epigenetic, transcriptional, and post-transcriptional levels. The interaction between TEs and these defense mechanisms has led to an evolutionary arms race where TEs are suppressed, evolve to escape suppression, then are suppressed again as the defense mechanisms undergo compensatory change. The result is complex and constantly evolving interactions between TEs and host genomes.

Keywords: Adaptation; Disease; Exaptation; Horizontal transfer; Mobile elements; Retrotransposons; TE defense; Transposons.

Fig. 1

Mammalian transposable elements. a Structure of common mammalian transposable elements. A and B box, promoter regions derived from 7SL RNA; FRAM, free right Alu monomer; FLAM, free left Alu monomer; A(n) poly A repeat; UTR, untranslated region; ORF0, primate-specific open reading frame 0; ORF1, nuclear chaperone protein; ORF2 reverse transcriptase; EN, endonuclease domain; RT, reverse transcriptase domain; AP-EN, apurinic-apyrimidinic endonuclease; U3, unique 3′ sequence; R, repeated sequence; U5, unique 5′ sequence; PBS, tRNA primer binding site; GAG, GAG protein; MA, matrix domain; CA, capsid domain; NC, nucleocapsid domain; POL, polyprotein; PR, protease domain; INT, integrase domain; RH, RNAse H domain; ENV, envelope protein; Rec/NP9, Rec and NP9 proteins including possible alternative splicing events; TIR, terminal inverted repeat; DNA-B, DNA binding domain; DDD, three conserved aspartate residues; TC, TC dinucleotide sequence; ZnF, zinc-finger-containing motifs; RepHel, replicase protein; Rep, replicase domain; Hel, helicase domain; CTAG -CTAG nucleotide sequence. b Representative elements drawn to scale

Fig. 2

Major transitions in TE content along are plotted along the mammalian phylogeny. The mammal phylogeny is modified from Meredith et al. (Meredith et al. 2011). Events were inferred to specific nodes using information from (Alföldi et al. ; Churakov et al. ; Gogolevsky et al. ; Gogolevsky et al. ; Green et al. ; Hillier et al. ; Kriegs et al. ; Lupan et al. ; Nikaido et al. ; Novick et al. ; Pace et al. ; Pagan et al. ; Pritham and Feschotte ; Ray et al. ; Ray et al. ; Rinehart et al. ; Shimamura et al. ; Smit et al. ; Suh et al. ; Vassetzky and Kramerov ; Walsh et al. ; Wang et al. ; Warren et al. 2008) and are generally classified into four categories. “Origination Events” (red) refer to the de novo or composite origin of new TEs. “Horizontal Transfer Events” (blue) refer to the horizontal transmission of TEs from non-mammalian lineages. “Reduction or Expansion Events” (green) refer to dramatic shifts in accumulation patterns. “Ancestral Elements” (pink) refer to elements that were present in the ancestral mammalian genome

Fig. 3

TE content in mammal and non-mammal vertebrate genomes. TE content was quantified from pre-masked genomes available at http://repeatmasker.org/genomicDatasets/RMGenomicDatasets.html (last accessed 30 November 2014). Genome size was estimated from the number of bases in the genome assembly