Genesis and regulatory wiring of retroelement-derived domesticated genes: A phylogenomic perspective

Molecular Biology and Evolution

Volumn 30, Issue 5, 2013, Pages 1015-1031

  Kokošar, Janez ^a   Kordiš, Dušan ^a  

^a JO EF STEFAN INSTITUTE   (Slovenia)

Author keywords

molecular domestication; neofunctionalization; phylogenomics; placentals; regulatory evolution; retroelement

Indexed keywords

CHORDATA; DOMESTICATED GENE; GENE; GENE DUPLICATION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENOMICS; PLACENTAL MAMMALS; PROMOTER REGION; RETROPOSON; REVIEW; UNTRANSLATED REGION;

ANIMALS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENOMICS; MAMMALS; PHYLOGENY; RETROELEMENTS;

AMNIOTA; EUKARYOTA; EUTHERIA; MAMMALIA; METAVIRIDAE; VERTEBRATA;

EID: 84876548744     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/mst014     Document Type: Review

References (79)

1. Almeida LM, Silva IT, Silva WA Jr, Castro JP, Riggs PK, Carareto CM, Amaral ME. 2007. The contribution of transposable elements to Bos taurus gene structure. Gene 390: 180-189.
2. Andreassi C, Riccio A. 2009. To localize or not to localize: mRNA fate is in 3'UTR ends. Trends Cell Biol. 19: 465-474.
3. Bao W, Kapitonov VV, Jurka J. 2010. Ginger DNA transposons in eukaryotes and their evolutionary relationships with long terminal repeat retrotransposons. Mob DNA. 1: 3.
4. Barrett LW, Fletcher S, Wilton SD. 2012. Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci. 69: 3613-3634.
5. Benton MJ, Twitchett RJ. 2003. How to kill (almost) all life: the end-Permian extinction event. Trends Ecol Evol. 18: 358-365. (Pubitemid 36774627)
6. Biémont C, Vieira C. 2006. Junk DNA as an evolutionary force. Nature 443: 521-524.
7. Bock C, Walter J, Paulsen M, Lengauer T. 2007. CpG island mapping by epigenome prediction. PLoS Comput Biol. 3: e110.
8. Brandt J, Schrauth S, Veith AM, Froschauer A, Haneke T, Schultheis C, Gessler M, Leimeister C, Volff JN. 2005. Transposable elements as a source of genetic innovation: expression and evolution of a family of retrotransposon- derived neogenes in mammals. Gene 345: 101-111. (Pubitemid 40208506)
9. Brandt J, Veith AM, Volff JN. 2005. A family of neofunctionalized Ty3/gypsy retrotransposon genes in mammalian genomes. Cytogenet Genome Res. 110: 307-317. (Pubitemid 41159908)
10. Britten R. 2006. Transposable elements have contributed to thousands of human proteins. Proc Natl Acad Sci USA. 103: 1798-1803. (Pubitemid 43228773)
11. Brosius J. 1999. RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene 238: 115-134. (Pubitemid 29436103)
12. Campillos M, Doerks T, Shah PK, Bork P. 2006. Computational characterization of multiple Gag-like human proteins. Trends Genet. 22: 585-589. (Pubitemid 44602270)
13. Castillo-Davis CI, Hartl DL, Achaz G. 2004. cis-Regulatory and protein evolution in orthologous and duplicate genes. Genome Res. 14: 1530-1536. (Pubitemid 39193403)
14. Churakov G, Kriegs JO, Baertsch R, Zemann A, Brosius J, Schmitz J. 2009. Mosaic retroposon insertion patterns in placental mammals. Genome Res. 19: 868-875.
15. de Parseval N, Heidmann T. 2005. Human endogenous retroviruses: from infectious elements to human genes. Cytogenet Genome Res. 110: 318-332. (Pubitemid 41159909)
16. Delsuc F, Brinkmann H, Philippe H. 2005. Phylogenomics and the reconstruction of the tree of life. Nat Rev Genet. 6: 361-375. (Pubitemid 40577180)
17. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797. (Pubitemid 38832724)
18. Eisen JA. 1998. Phylogenomics: improving functional predictions for uncharacterized genes by evolutionary analysis. Genome Res. 8: 163-167. (Pubitemid 28177226)
19. Emerson JJ, Kaessmann H, Betran E, Long M. 2004. Extensive gene traffic on the mammalian X chromosome. Science 303: 537-540. (Pubitemid 38120854)
20. Emerson RO, Thomas JH. 2011. Gypsy and the birth of the SCAN domain. J Virol. 85: 12043-12052.
21. Fablet M, Bueno M, Potrzebowski L, Kaessmann H. 2009. Evolutionary origin and functions of retrogene introns. Mol Biol Evol. 26: 2147-2156.
22. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 9: 397-405. (Pubitemid 351556062)
23. Feschotte C, Pritham EJ. 2007. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet. 41: 331-368.
24. Gertz EM, Yu YK, Agarwala R, Schäffer AA, Altschul SF. 2006. Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol. 4: 41.
25. Gorinsek B, Gubensek F, Kordis D. 2004. Evolutionary genomics of chromoviruses in eukaryotes. Mol Biol Evol. 21: 781-798. (Pubitemid 38529721)
26. Gorinsek B, Gubensek F, Kordis D. 2005. Phylogenomic analysis of chromoviruses. Cytogenet Genome Res. 110: 543-552. (Pubitemid 41159931)
27. Gotea V, Makalowski W. 2006. Do transposable elements really contribute to proteomes? Trends Genet. 22: 260-267.
28. Grillo G, Turi A, Licciulli F, et al. (11 co-authors). 2010. UTRdb and UTRsite (RELEASE 2010): a collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res. 38(Database issue): D75-D80.
29. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33(Web Server issue): W557-W559. (Pubitemid 44529983)
30. Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755.
31. Jurka J, Kapitonov VV, Kohany O, JurkaMV. 2007. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genomics Hum Genet. 8: 241-259.
32. Kaessmann H. 2010. Origins, evolution, and phenotypic impact of new genes. Genome Res. 20: 1313-1326.
33. Kaessmann H, Vinckenbosch N, Long M. 2009. RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet. 10: 19-31.
34. Kalitsis P, Saffery R. 2009. Inherent promoter bidirectionality facilitates maintenance of sequence integrity and transcription of parasitic DNA in mammalian genomes. BMC Genomics 10: 498.
35. Kaneko-Ishino T, Ishino F. 2012. The role of genes domesticated from LTR retrotransposons and retroviruses in mammals. Front Microbiol. 3: 262.
36. Kazazian HH Jr. 2004. Mobile elements: drivers of genome evolution. Science 303: 1626-1632. (Pubitemid 38338313)
37. KidwellMG, Lisch DR. 2001. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55: 1-24. (Pubitemid 32175281)
38. Korb E, Finkbeiner S. 2011. Arc in synaptic plasticity: from gene to behavior. Trends Neurosci. 34: 591-598.
39. Kordis D. 2005. A genomic perspective on the chromodomaincontaining retrotransposons: chromoviruses. Gene 347: 161-173. (Pubitemid 40403756)
40. Kordis D. 2009. Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet Genome Res. 127: 94-111.
41. Kordis D. 2011. Extensive intron gain in the ancestor of placental mammals. Biol Direct. 6: 59.
42. Kordis D, Kokosar J. 2012. What can domesticated genes tell us about the intron gain in mammals? Int J Evol Biol. 2012: 27898.
43. Kordis D, Lovsin N, Gubensek F. 2006. Phylogenomic analysis of the L1 retrotransposons in Deuterostomia. Syst Biol. 55: 886-901.
44. Krull M, Petrusma M, Makalowski W, Brosius J, Schmitz J. 2007. Functional persistence of exonized mammalian-wide interspersed repeat elements (MIRs). Genome Res. 17: 1139-1145. (Pubitemid 47204857)
45. Llorens C, Marin I. 2001. A mammalian gene evolved from the integrase domain of an LTR retrotransposon. Mol Biol Evol. 18: 1597-1600. (Pubitemid 32735108)
46. Long M, Betran E, Thornton K,Wang W. 2003. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 4: 865-875. (Pubitemid 37345613)
47. Lynch C, Tristem M. 2003. A co-opted gypsy-type LTR-retrotransposon is conserved in the genomes of humans, sheep, mice, and rats. Curr Biol. 13: 1518-1523. (Pubitemid 37078408)
48. Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290: 1151-1155.
49. Maglott D, Ostell J, Pruitt KD, Tatusova T. 2011. Entrez gene: genecentered information at NCBI. Nucleic Acids Res. 39(Database issue): D52-D57.
50. Marco A, Marn I. 2009. CGIN1: a retroviral contribution to mammalian genomes. Mol Biol Evol. 26: 2167-2170.
51. Marn I. 2010. GIN transposons: genetic elements linking retrotransposons and genes. Mol Biol Evol. 27: 1903-1911.
52. Mariño-Raḿrez L, Lewis KC, Landsman D, Jordan IK. 2005. Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res. 110: 333-341. (Pubitemid 41159910)
53. Matsui T, Miyamoto K, Kubo A, et al. (12 co-authors). 2011. SASPase regulates stratum corneum hydration through profilaggrin-tofilaggrin processing. EMBO Mol Med. 3: 320-333.
54. Medstrand P, van de Lagemaat LN, Dunn CA, Landry JR, Svenback D, Mager DL. 2005. Impact of transposable elements on the evolution of mammalian gene regulation. Cytogenet Genome Res. 110: 342-352. (Pubitemid 41159911)
55. Meredith RW, Janecka JE, Gatesy J, et al. (22 co-authors). 2011. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334: 521-524.
56. Mi S, Lee X, Li X, et al. (12 co-authors). 2000. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403: 785-789. (Pubitemid 30111841)
57. Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE); 2010 Nov 14, New Orleans, LA.
58. Miller WJ, McDonald JF, Nouaud D, Anxolabéhére D. 1999. Molecular domestication-more than a sporadic episode in evolution. Genetica 107: 197-207. (Pubitemid 129574966)
59. Muffato M, Louis A, Poisnel CE, Roest Crollius H. 2010. Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes. Bioinformatics 26: 1119-1121.
60. Nekrutenko A, Li WH. 2001. Transposable elements are found in a large number of human protein-coding genes. Trends Genet. 17: 619-621. (Pubitemid 32973815)
61. Nishihara H, Maruyama S, Okada N. 2009. Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci USA. 106: 5235-5240.
62. Oldham MC, Horvath S, Geschwind DH. 2006. Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci USA. 103: 17973-17978. (Pubitemid 44852270)
63. Pruitt KD, Tatusova T, Klimke W, Maglott DR. 2009. NCBI reference sequences: current status, policy and new initiatives. Nucleic Acids Res. 37(Database issue): D32-D36.
64. Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
65. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 4: 406-425.
66. Schmitz J, Brosius J. 2011. Exonization of transposed elements: a challenge and opportunity for evolution. Biochimie 93: 1928-1934.
67. Schüller M, Jenne D, Voltz R. 2005. The human PNMA family: novel neuronal proteins implicated in paraneoplastic neurological disease. J Neuroimmunol. 169: 172-176. (Pubitemid 41527102)
68. She X, Rohl CA, Castle JC, Kulkarni AV, Johnson JM, Chen R. 2009. Definition, conservation and epigenetics of housekeeping and tissue-enriched genes. BMC Genomics 10: 269.
69. Shiao MS, Khil P, Camerini-Otero RD, Shiroishi T, Moriwaki K, Yu HT, Long M. 2007. Origins of new male germ-line functions from X-derived autosomal retrogenes in the mouse. Mol Biol Evol. 24: 2242-2253. (Pubitemid 47574724)
70. Sinzelle L, Izsvak Z, Ivics Z. 2009. Molecular domestication of transposable elements: from detrimental parasites to useful host genes. Cell Mol Life Sci. 66: 1073-1093.
71. Sorek R. 2007. The birth of new exons: mechanisms and evolutionary consequences. RNA 13: 1603-1608. (Pubitemid 47481668)
72. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 123: 1133-1146. (Pubitemid 41785426)
73. Takaji M, Komatsu Y, Watakabe A, Hashikawa T, Yamamori T. 2009. Paraneoplastic antigen-like 5 gene (PNMA5) is preferentially expressed in the association areas in a primate specific manner. Cereb Cortex. 19: 2865-2879.
74. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28: 2731-2739.
75. Thornburg BG, Gotea V,MakalowskiW. 2006. Transposable elements as a significant source of transcription regulating signals. Gene 365: 104-110. (Pubitemid 43185230)
76. Vinckenbosch N, Dupanloup I, Kaessmann H. 2006. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA. 103: 3220-3225. (Pubitemid 43346451)
77. Volff JN. 2006. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28: 913-922.
78. Yamamori T. 2011. Selective gene expression in regions of primate neocortex: implications for cortical specialization. Prog Neurobiol. 94: 201-222.
79. Zdobnov EM, Campillos M, Harrington ED, Torrents D, Bork P. 2005. Protein coding potential of retroviruses and other transposable elements in vertebrate genomes. Nucleic Acids Res. 33: 946-954. (Pubitemid 41430515)