Evolutionary Emergence of Genes Through Retrotransposition

Abstract

Variation in the number of genes among species indicates that new genes are continuously generated over evolutionary times. Evidence is accumulating that transposable elements, including retrotransposons (which account for about 90% of all transposable elements inserted in primate genomes), are potent mediators of new gene origination. Retrotransposons have fostered genetic innovation during human and primate evolution through: (i) alteration of structure and/or expression of pre‚Äźexisting genes following their insertion, (ii) recruitment (or domestication) of their coding sequence by the host genome and (iii) their ability to mediate gene duplication via ectopic recombination, sequence transduction and gene retrotransposition.

Keywords: retrotransposons; genetic innovation; recruitment; gene duplication; primate evolution

Figure 1.

Structures of four typical human retrotransposons (not drawn to scale). The Alu element consists of two 7SL RNA‐related monomers separated by an A‐rich connector; the left monomer contains A and B boxes (grey boxes) promoting transcription by RNA polymerase III. The L1 element consists of two open reading frames (ORF1 and ORF2) surrounded by 5′ and 3′ untranslated regions (UTR). The SVA element consists of a region derived from a SINE‐R element and an Alu‐like region separated by a variable number of tandem repeats (VNTR). All three elements end with a poly A tail (AAA). Alu and SVA elements are nonautonomous retrotransposons that hijack the molecular retrotransposition machinery of the autonomous L1 element to mediate their own retrotransposition. The HERV element consists of three genes (gag, pol and env) surrounded by long terminal repeats (LTR). All four elements generate target site duplications (black arrows) upon insertion.

Figure 2.

Schematic phylogenetic tree of the primate order. Names and approximate evolutionary age of the major lineages discussed in the main text are shown.

Figure 3.

Alteration of gene structure mediated by Alu retrotransposons. (a) Alu exonization: a hypothetical gene constituted of three exons (light grey, white and dark grey boxes) is shown with its splicing pattern (dashed lines above gene). Activation of the cryptic donor (d) and acceptor (a) splice sites of an Alu element (black arrow) inserted in opposite orientation relative to gene transcription in the first intron leads to integration of noncoding Alu sequence in the gene's transcript (dashed lines below gene) and conversion to coding sequence. (b) Ectopic recombination: a hypothetical gene constituted of three exons (light grey, white and dark grey boxes) is shown on top with its splicing pattern (dashed lines). Ectopic recombination (crossed thin lines) between two intronic Alu elements (dashed arrows) leads to the deletion of the intervening sequence containing the entire white exon (middle). As a result (bottom), the gene is now constituted by two exons (light and dark grey) with a new splicing pattern (dashed lines).

Figure 4.

Retrotransposon‐mediated sequence transduction. A hypothetical gene constituted of two exons (light and dark grey boxes) and an upstream L1 retrotransposon (black arrow) are shown on top with their respective polyadenylation motifs (pA) signalling transcription termination. RNA transcription starts at the 5′ end of the L1 element (thin horizontal arrow) and normally proceeds down to the L1 polyadenylation signal, resulting in transcription termination. The transcript (middle) therefore consists of the L1 RNA sequence ending with a poly A tail (AAA), which can subsequently be integrated into the genome by retrotransposition. Sometimes, the L1 polyadenylation signal is ignored and transcription proceeds down to another polyadenylation signal located in the L1 flanking sequence. The transcript therefore consists of the L1 RNA sequence, followed by the downstream sequence flanking the L1 element and a poly A tail (bottom). In this example, the downstream sequence contains a gene which intron is being spliced out (dashed lines) before transcript integration into the genome by retrotransposition, resulting in the duplication of the L1 element and an intronless version of the original gene.

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Further Reading

Batzer MA and Deininger PL (2002) Alu repeats and human genomic diversity. Nature Reviews Genetics 3: 370–379.

Chen JM, Stenson PD, Cooper DN and Ferec C (2005) A systematic analysis of LINE‐1 endonuclease‐dependent retrotranspositional events causing human genetic disease. Human Genetics 117: 411–427.

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Volff JN (2006) Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28: 913–922.

Wang H, Xing J, Grover D et al. (2005) SVA elements: a hominid specific retroposon family. Journal of Molecular Biology 354: 994–1007.

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How to Cite close
Cordaux, Richard, and Batzer, Mark A(Mar 2008) Evolutionary Emergence of Genes Through Retrotransposition. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020783]