Evolutionary Emergence of Genes Through Retrotransposition


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 (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 (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.



Bailey JA, Liu G and Eichler EE (2003) An Alu transposition model for the origin and expansion of human segmental duplications. American Journal of Human Genetics 73: 823–834.

Blaise S, de Parseval N, Bénit L and Heidmann T (2003) Genome‐wide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proceedings of the National Academy of Sciences of the USA 100: 13013–13018.

Burki F and Kaessmann H (2004) Birth and adaptive evolution of a hominoid gene that supports high neurotransmitter flux. Nature Genetics 36: 1061–1063.

Cordaux R, Udit S, Batzer MA and Feschotte C (2006) Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. Proceedings of the National Academy of Sciences of the USA 103: 8101–8106.

Johnson ME, Viggiano L, Bailey JA et al. (2001) Positive selection of a gene family during the emergence of humans and African apes. Nature 413: 514–519.

van de Lagemaat LN, Landry JR, Mager DL and Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends in Genetics 19: 530–536.

Marques AC, Dupanloup I, Vinckenbosch N, Reymond A and Kaessmann H (2005) Emergence of young human genes after a burst of retroposition in primates. PLoS Biology 3: e357.

Mi S, Lee X, Li X et al. (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403: 785–789.

Moran JV, DeBerardinis RJ and Kazazian HH Jr (1999) Exon shuffling by L1 retrotransposition. Science 283: 1530–1534.

Nekrutenko A and Li WH (2001) Transposable elements are found in a large number of human protein‐coding genes. Trends in Genetics 17: 619–621.

Perepelitsa‐Belancio V and Deininger P (2003) RNA truncation by premature polyadenylation attenuates human mobile element activity. Nature Genetics 35: 363–366.

Sen SK, Han K, Wang J et al. (2006) Human genomic deletions mediated by recombination between Alu elements. American Journal of Human Genetics 79: 41–53.

Sorek R, Ast G and Graur D (2002) Alu‐containing exons are alternatively spliced. Genome Research 12: 1060–1067.

Wheelan SJ, Aizawa Y, Han JS and Boeke JD (2005) Gene‐breaking: a new paradigm for human retrotransposon‐mediated gene evolution. Genome Research 15: 1073–1078.

Xing J, Wang H, Belancio VP et al. (2006) Emergence of primate genes by retrotransposon‐mediated sequence transduction. Proceedings of the National Academy of Sciences of the USA 103: 17608–17613.

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.

Craig NL, Craigie R, Gellert M and Lambowitz AM (2002) Mobile DNA II. Washington, DC: American Society for Microbiology Press.

International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409: 860–921.

Jacob F (1977) Evolution and tinkering. Science 196: 1161–1166.

Long M, Betran E, Thornton K and Wang W (2003) The origin of new genes: glimpses from the young and old. Nature Reviews Genetics 4: 865–875.

Ostertag EM and Kazazian HH Jr (2001) Biology of mammalian L1 retrotransposons. Annual Reviews of Genetics 35: 501–538.

de Parseval N and Heidmann T (2005) Human endogenous retroviruses: from infectious elements to human genes. Cytogenetic and Genome Research 110: 318–332.

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.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

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]