Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates

Genome Biology and Evolution

Volumn 7, Issue 2, 2015, Pages 567-580

  Chalopin, Domitille ^a   Naville, Magali ^a   Plard, Floriane ^b   Galiana, Delphine ^a   Volff, Jean Nicolas ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

genome size; mobile DNA; retrotransposon; transposon

Indexed keywords

AVES; DANIO RERIO; MAMMALIA; ORYZIINAE; TELEOSTEI; TETRAODON; TETRAODONTIDAE; VERTEBRATA;

RETROPOSON; TRANSPOSON;

ANIMAL; COMPARATIVE STUDY; FISH; GENETIC VARIABILITY; GENETICS; GENOME; GENOME SIZE; LONG INTERSPERSED REPEAT; MOLECULAR EVOLUTION; PHYLOGENY; RETROPOSON; SHORT INTERSPERSED REPEAT; TRANSPOSON; VERTEBRATE;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; FISHES; GENETIC VARIATION; GENOME; GENOME SIZE; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; PHYLOGENY; RETROELEMENTS; SHORT INTERSPERSED NUCLEOTIDE ELEMENTS; VERTEBRATES;

EID: 84928236059     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv005     Document Type: Article

References (111)

1. Abrusán G, Krambeck HJ. 2006. Competition may determine the diversity of transposable elements. Theor Popul Biol. 70:364-375.
2. Agrawal A, Eastman QM, Schatz DG. 1998. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394:744-751.
3. Ågren JA, Wright SI. 2011. Co-evolution between transposable elements and their hosts: a major factor in genome size evolution? Chromosome Res. 19:777-786.
4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403-410.
5. Amemiya CT, et al. 2013. The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311-316.
6. Bao W, Jurka J. 2008. EnSpm DNA transposons in Zebrafish. Repbase Reports 8:823.
7. Basta HA, Buzak AJ, McClure MA. 2007. Identification of novel retroid agents in Danio rerio, Oryzias latipes, Gasterosteus aculeatus and Tetraodon nigroviridis. Evol Bioinform Online. 3:179-195.
8. Blass E, Bell M, Boissinot S. 2012. Accumulation and rapid decay of non- LTR retrotransposons in the genome of the three-spine stickleback. Genome Biol Evol. 4:687-702.
9. Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN. 2008. Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res. 16:203-215.
10. Böhne A, et al. 2012. Zisupton - a novel superfamily of DNA transposable elements recently active in fish. Mol Biol Evol. 29:631-645.
11. Bosco G, Campbell P, Leiva-Neto JT, Markov TA. 2007. Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177:1277-1290.
12. Brookfield JFY. 2011. Host-parasite relationships in the genome. BMC Biol. 9:67.
13. Burns KH, Boeke JD. 2012. Human transposon tectonics. Cell 149: 740-752.
14. Castoe TA, et al. 2011. Discovery of highly divergent repeat landscapes in snake genomes using high-throughput sequencing. Genome Biol Evol. 3:641-653.
15. Chalopin D, et al. 2013. Evolutionary active transposable elements in the genome of the coelacanth. J Exp Zool B Mol Dev Evol. 322: 322-333.
16. Dalloul RA, et al. 2010. Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): genome assembly and analysis. PLoS Biol. 8:e1000475.
17. Dasilva C, et al. 2002. Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome. Proc Natl Acad Sci U S A. 99: 13636-13641.
18. De Koning AP, GuW, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 7:e1002384.
19. De la Chaux N, Wagner A. 2011. BEL/Pao retrotransposons in metazoan genomes. BMC Evol Biol. 11:154.
20. Deininger PL, Moran JV, Batzer MA, Kazazian HH Jr. 2003. Mobile elements and mammalian genome evolution. Curr Opin Genet Dev. 13: 651-658.
21. Díaz-Uriarte R, Garland T Jr. 1998. Effects of branch length errors on the performance of phylogenetically independent contrasts. Syst Biol. 47: 654-672.
22. Dufresne F, Jeffery N. 2011. A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Res. 19: 925-938.
23. Duvernell DD, Pryor SR, Adams SM. 2004. Teleost fish genomes contain a diverse array of L1 retrotransposon lineages that exhibit a low copy number and high rate of turnover. J Mol Evol. 59:298-308.
24. Eickbush TH, Jamburuthugoda VK. 2008. The diversity of retrotransposons and the properties of their reverse transcriptases. Virus Res. 134: 221-234.
25. Ellegren H, et al. 2012. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491:756-760.
26. Ellison CE, Bachtrog D. 2013. Dosage compensation via transposable element mediated rewiring of a regulatory network. Science 342: 846-850.
27. Evgen'ev MB. 2013. What happens when Penelope comes?: an unusual retroelement invades a host species genome exploring different strategies. Mob Genet Elements 3:e24542.
28. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat. 125:1-15.
29. Feschotte C. 2004. Merlin, a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Mol Biol Evol. 21:1769-1780.
30. Feschotte C. 2008. Transposable elements and the evolution of regulatory networks. Nat Rev Genet. 9:397-405.
31. Feschotte C, Pritham EJ. 2005. Non-mammalian c-integrases are encoded by giant transposable elements. Trends Genet. 21:551-552.
32. Feschotte C, Pritham EJ. 2007. DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet. 41:331-368.
33. Finnegan DJ. 1989. Eukaryotic transposable elements and genome evolution. Trends Genet. 5:103-107.
34. Fischer C, et al. 2005. Diversity and clustered distribution of retrotransposable elements in the compact genome of the pufferfish Tetraodon nigroviridis. Cytogenet Genome Res. 110:522-536.
35. Furano AV, Duvernell D, Boissinot S. 2004. L1 (LINE-1) retrotransposon diversity differs dramatically between mammals and fish. Trends Genet. 20:9-14.
36. Gifford R, Tristem M. 2003. The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291-315.
37. Gilbert C, Hernandez SS, Flores-Benabib J, Smith EN, Feschotte C. 2012. Rampant horizontal transfer of SPIN transposons in squamate reptiles. Mol Biol Evol. 29:503-515.
38. Gilbert C, Waters P, Feschotte C, Schaack S. 2013. Horizontal transfer of OC1 transposons in the Tasmanian devil. BMC Genomics 14:134.
39. Goodier JL, Kazazian HH Jr. 2008. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135:23-35.
40. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 27:221-224.
41. Gregory TR. 2001. The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells Mol Dis. 27: 830-843.
42. Hancks DC, Kazazian HH Jr. 2012. Active human retrotransposons: variation and disease. Curr Opin Genet Dev. 22:191-203.
43. Hancock JM. 2002. Genome size and the accumulation of simple repeats: implications of new data from genome sequencing projects. Genetica 115:93-103.
44. Hedges SB, Dudley J, Kumar S. 2006. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972.
45. Hiom K, Melek M, Gellert M. 1998. DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94: 463-470.
46. Huang Y, et al. 2013. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat Genet. 45: 776-783.
47. Jacques PÉ, Jeyakani J, Bourque G. 2013. The majority of primate-specific regulatory sequences are derived from transposable elements. PLoS Genet. 9:e1003504.
48. Jaillon O, et al. 2004. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431: 946-957.
49. Jones FC, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
50. Jurka J. 2000. Repbase Update: a database and an electronic journal of repetitive elements. Trends Genet. 16:418-420.
51. Jurka J, Klonowski P, Dagman V, Pelton P. 1996. CENSOR - a program for identification and elimination of repetitive elements from DNA sequences. Comput Chem. 20:119-121.
52. Kapitonov VV, Jurka J. 2001. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci U S A. 98:8714-8719.
53. Kapitonov VV, Jurka J. 2005. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3:e181.
54. Kapitonov VV, Jurka J. 2006. Self-synthesizing DNA transposons in eukaryotes. Proc Natl Acad Sci U S A. 103:4540-4545.
55. Kapitonov VV, Jurka J. 2009. R2 non-LTR retrotransposons in the bird genome. Repbase Rep. 9:1329.
56. Kapusta A, et al. 2013. Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet. 9:e1003470.
57. Kazazian HH Jr. 2004. Mobile elements: drivers of genome evolution. Science 303:1626-1632.
58. Kidwell MG. 2002. Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49-63.
59. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16:111-120.
60. Kojima KK, Jurka J. 2011. Crypton transposons: identification of new diverse families and ancient domestication events. Mob DNA 2:12.
61. Kojima KK, Jurka J. 2013a. Non-LTR retrotransposons from green anole. Repbase Rep. 4:1615.
62. Kojima KK, Jurka J. 2013b. Non-LTR retrotransposons from the western painted turtle. Repbase Rep. 9:2217.
63. Kordis D. 2009. Transposable elements in reptilian and avian (sauropsida) genomes. Cytogenet Genome Res. 127:94-111.
64. Kordis D, Gubensek F. 1999. Horizontal transfer of non-LTR retrotransposons in vertebrates. Genetica 107:121-128.
65. Kuraku S, Qiu H, Meyer A. 2012. Horizontal transfers of Tc1 elements between teleost fishes and their vertebrate parasites, lampreys. Genome Biol Evol. 4:929-936.
66. Le Rouzic A, Capy P. 2005. The first step of transposable elements invasion: parasitic strategy vs. genetic drift. Genetics 169:1033-1043.
67. Le Rouzic A, Capy P. 2006. Population genetics models of competition between transposable element subfamilies. Genetics 174:785-793.
68. Le Rouzic A, Capy P. 2009. Theorical approaches to the dynamics of transposable elements in genomes, populations, and species. Genome Dyn Stab. 4:1-19.
69. Levin HL, Moran JV. 2011. Dynamic interactions between transposable elements and their hosts. Nat Rev Genet. 12:615-627.
70. Luchetti A, Mantovani B. 2013. Non-LTR R2 element evolutionary patterns: phylogenetic incongruences, rapid radiation and the maintenance of multiple lineages. PLoS One 8:e57076.
71. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302:1401-1404.
72. Malik HS, Burke WD, Eickbush TH. 1999. The age and evolution of non- LTR retrotransposable elements. Mol Biol Evol. 16:793-805.
73. Metcalfe CJ, Casane D. 2013. Accommodating the load: the transposable element content of very large genomes. Mob Genet Elements 3: e24775.
74. Nelson JS. 2006. Fishes of the world. New York: John Wiley and Sons.
75. Novick P, Smith J, Ray D, Boissinot S. 2010. Independent and parallel lateral transfer of DNA transposons in tetrapod genomes. Gene 449: 85-94.
76. Novick PA, Basta H, Floumanhaft M, McClure MA, Boissinot S. 2009. The evolutionary dynamics of autonomous non-LTR retrotransposons in the lizard Anolis carolinensis shows more similarity to fish than mammals. Mol Biol Evol. 26:1811-1822.
77. Ogiwara I, Miya M, Ohshima K, Okada N. 2002. V-SINEs: a new superfamily of vertebrate SINEs that are widespread in vertebrate genomes and retain a strongly conserved segment within each repetitive unit. Genome Res. 12:316-324.
78. Oliveira SG, Bao W, Martins C, Jurka J. 2012. Horizontal transfers of Mariner transposons between mammals and insects. Mob DNA 3:14.
79. Pace JK, Gilbert C, Clark MS, Feschotte C. 2008. Repeated horizontal transfer of a DNA transposons in mammals and other tetrapods. Proc Natl Acad Sci U S A. 105:17023-17028.
80. Parfrey LW, Lahr DJG, Katz LA. 2008. The dynamic nature of eukaryotic genomes. Mol Biol Evol. 25:787-794.
81. Petrov DA. 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17:23-28.
82. Piskurek O, Jackson DJ. 2011. Tracking the ancestry of a deeply conserved eumetazoan SINE domain. Mol Biol Evol. 28:2727-2730.
83. Piskurek O, Okada N. 2007. Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals. Proc Natl Acad Sci U S A. 104:12046-12051.
84. Poulter RT, Goodwin TJ. 2005. DIRS-1 and the other tyrosine recombinase retrotransposons. Cytogenet Genome Res. 110:575-588.
85. Pritham EJ, Feschotte C. 2007. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc Natl Acad Sci U S A. 104:1895-1900.
86. Ravi V, Venkatesh B. 2008. Rapidly evolving fish genomes and teleost diversity. Curr Opin Genet Dev. 18:544-550.
87. Rebollo R, Romanish MT, Mager DL. 2012. Transposable elements: an abundant and natural source of regulatory sequences for host genes. Annu Rev Genet. 46:21-42.
88. Sarropoulou E, Fernandes JM. 2011. Comparative genomics in teleost species: knowledge transfer by linking the genomes of model and non-model fish species. Comp Biochem Physiol Part D Genomics Proteomics. 6:92-102.
89. Schartl M, et al. 2013. The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nat Genet. 45:567-572.
90. Sievers F, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 7: 539.
91. Sormacheva I, et al. 2012. Vertical evolution and horizontal transfer of CR1 non-LTR retrotransposons and Tc1/mariner DNA transposons in Lepidoptera species. Mol Biol Evol. 29:3685-3702.
92. Stanke M, Steinkamp R, Waack S, Morgenstern B. 2004. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32: 309-312.
93. Sun C, et al. 2012. LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders. Genome Biol Evol. 4: 168-183.
94. Syvanen M. 2012. Evolutionary implications of horizontal gene transfer. Annu Rev Genet. 46:341-358.
95. Thomas J, Sorourian M, Ray D, Baker RJ, Pritham EJ. 2011. The limited distribution of Helitrons to vesper bats supports horizontal transfer. Gene 474:52-58.
96. Tollis M, Boissinot S. 2013. Lizards and LINEs: selection and demography affect the fate of L1 retrotransposons in the genome of the green anole (Anolis carolinensis). Genome Biol Evol. 5: 1754-1768.
97. Vieira C, Lepetit D, Dumont S, Biémont C. 1999. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol. 16:1251-1255.
98. Vieira C, Nardon C, Arpin C, Lepetit D, Biémont C. 2002. Evolution of genome size in Drosophila. Is the invader's genome being invaded by transposable elements? Mol Biol Evol. 19:1154-1161.
99. Volff JN. 2005. Genome evolution and biodiversity in teleost fish. Heredity 94:280-294.
100. Volff JN. 2006. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28: 913-922.
101. Volff JN, Bouneau L, Ozouf-costaz C, Fischer C. 2003. Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet. 19:674-678.
102. Volff JN, Körting C, Froschauer A, Sweeney K, Schartl M. 2001. Non-LTR retrotransposons encoding a restriction enzyme-like endonuclease in vertebrates. J Mol Evol. 52:351-360.
103. Vorechovsky I. 2010. Transposable elements in disease-associated cryptic exons. Hum Genet. 127:135-154.
104. Wallau GL, Ortiz MF, Loreto EL. 2012. Horizontal transposons transfer in Eukarya: detection, bias and perspectives. Genome Biol Evol. 4: 801-811.
105. Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL. 2013. Widespread horizontal transfer of retrotransposons. Proc Natl Acad Sci U S A. 110:1012-1016.
106. Wicker T, et al. 2007. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 8:973-982.
107. Wittbrodt J, Shima A, Schartl M. 2002. Medaka - a model organism from the far East. Nat Rev Genet. 3:53-64.
108. Xie M, et al. 2013. DNA hypomethylation within specific transposable element families associates with tissue-specific enhancer landscape. Nat Genet. 45:836-841.
109. Yi S, Streelman JT. 2005. Genome size is negatively correlated with effective population size in ray-finned fish. Trends Genet. 21: 643-646.
110. Yohn CT, et al. 2005. Lineage-specific expansions of retroviral insertions within the genomes of African great apes but not humans and orangutans. PLoS Biol. 3:e110.
111. Zhan X, et al. 2013. Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle. Nat Genet. 45:563-566.