Evolvability, epigenetics and transposable elements

Biomolecular Concepts

Volumn 2, Issue 5, 2011, Pages 333-341

  Fablet, Marie ^a   Vieira, Cristina ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

environment; genome evolution; natural populations

Indexed keywords

EID: 84870196155     PISSN: 18685021     EISSN: 1868503X     Source Type: Journal    
DOI: 10.1515/BMC.2011.035     Document Type: Review

References (84)

1. Johannes F, Colomé-Tatché M. Concerning epigenetics and inbreeding. Nat Rev Genet 2011a; 12: 376.
2. Johannes F, Colomé-Tatché M. Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 2011b; 188: 215-227.
3. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 2007; 8: 272-285.
4. Huda A, Jordan IK. Epigenetic regulation of mammalian genomes by transposable elements. Annals of the New York Academy of Sciences 2009; 1178: 276-284.
5. Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R. Role of transposable elements in heterochromatin and epigenetic control. Nature 2004; 430: 471-476.
6. Yao S, Sukonnik T, Kean T, Bharadwaj RR, Pasceri P, Ellis J. Retrovirus silencing, variegation, extinction, and memory are controlled by a dynamic interplay of multiple epigenetic modifications. Mol Ther 2004; 10: 27-36.
7. Thomas CA Jr. The genetic organization of chromosomes. Annu Rev Genet 1971; 5: 237-256.
8. Biémont C, Vieira C. Junk DNA as an evolutionary force. Nature 2006; 443: 521-524.
9. Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006; 443: 931-949.
10. Nene V, Wortman J.R., Lawson D, Haas B, Kodira C, Tu Z, Loftus B, Xi Z, Megy K, Grabherr M, Ren Q, Zdobnov EM, Lobo NF, Campbell KS, Brown SE, Bonaldo MF, Zhu J, Sinkins SP, Hogenkamp DG, Amedeo P, Arensburger P, Atkinson PW, Bidwell S, Biedler J, Birney E, Bruggner RV, Costas J, Coy MR, Crabtree J, Crawford M, deBruyn B, DeCaprio D, Eiglmeier K, Eisenstadt E, El-Dorry H, Gelbart WM, Gomes SL, Hammond M, Hannick LI, Hogan J.R., Holmes MH, Jaffe D, Johnston JS, Kennedy RC, Koo H, Kravitz S, Kriventseva EV, Kulp D, LaButti K, Lee E, Li S, Lovin DD, Mao C, Mauceli E, Menck CFM, Miller J.R., Montgomery P, Mori A, Nascimento AL, Naveira HF, Nusbaum C, OLeary S, Orvis J, Pertea M, Quesneville H, Reidenbach KR, Rogers Y-H, Roth CW, Schneider J.R., Schatz M, Shumway M, Stanke M, Stinson EO, Tubio JMC, VanZee JP, Verjovski-Almeida S, Werner D, White O, Wyder S, Zeng Q, Zhao Q, Zhao Y, Hill CA, Raikhel AS, Soares MB, Knudson DL, Lee NH, Galagan J, Salzberg SL, Paulsen IT, Dimopoulos G, Collins FH, Birren B, Fraser-Liggett CM, Severson DW. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007; 316: 1718-1723.
11. International Silkworm Genome Consortium. The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 2008; 38: 1036-1045.
12. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, Antelo B, Bartholomay L, Bidwell S, Caler E, Camara F, Campbell CL, Campbell KS, Casola C, Castro MT, Chandramouliswaran I, Chapman SB, Christley S, Costas J, Eisenstadt E, Feschotte C, Fraser-Liggett C, Guigo R, Haas B, Hammond M, Hansson BS, Hemingway J, Hill S.R., Howarth C, Ignell R, Kennedy RC, Kodira CD, Lobo NF, Mao C, Mayhew G, Michel K, Mori A, Liu N, Naveira H, Nene V, Nguyen N, Pearson MD, Pritham EJ, Puiu D, Qi Y, Ranson H, Ribeiro JM, Roberston HM, Severson DW, Shumway M, Stanke M, Strausberg RL, Sun C, Sutton G, Tu ZJ, Tubio JM, Unger MF, Vanlandingham DL, Vilella AJ, White O, White J.R., Wondji CS, Wortman J, Zdobnov EM, Birren B, Christensen BM, Collins FH, Cornel A, Dimopoulos G, Hannick LI, Higgs S, Lanzaro GC, Lawson D, Lee NH, Muskavitch M.A., Raikhel AS, Atkinson PW. Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 2010; 330: 86-88.
13. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal M.A., Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan J.R., Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez J.R., Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, OBrochta D.A., Pfannkoch C, Qi R, Regier M.A., Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman J.R., Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL. The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002; 298: 129-149.
14. Dowsett AP, Young MW. Differing levels of dispersed repetitive DNA among closely related species of Drosophila. Proc Natl Acad Sci USA 1982; 79: 4570-4574.
15. Drosophila 12 Genomes Consortium. Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007; 450: 203-218.
16. Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet 1989; 5: 103-107.
17. Bergman CM, Quesneville H, Anxolabéhére D, Ashburner M. Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 2006; 7: R112.
18. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, The Nasonia Genome Working Group. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010; 327: 343-348.
19. Osanai-Futahashi M, Suetsugu Y, Mita K, Fujiwara H. Genome-wide screening and characterization of transposable elements and their distribution analysis in the silkworm, Bombyx mori. Insect Biochem Mol Biol 2008; 38: 1046-1057.
20. Tu Z, Coates C. Mosquito transposable elements. Insect Biochem Mol Biol 2004; 34: 631-644.
21. Boulesteix M, Biémont C. Transposable elements in mosquitoes. Cytogenet Genome Res 2005; 110: 500-509.
22. Aquadro CF, Lado KM, Noon WA. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence. Genetics 1988; 119: 875-888.
23. Nolte V, Schlötterer C. African Drosophila melanogaster and D. simulans populations have similar levels of sequence variability, suggesting comparable effective population sizes. Genetics 2008; 178: 405-412.
24. Loreto ELS, Carareto CMA, Capy P. Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 2008; 100: 545-554.
25. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C, Pan G, Xu J, Liu C, Lin Y, Qian J, Hou Y, Wu Z, Li G, Pan M, Li C, Shen Y, Lan X, Yuan L, Li T, Xu H, Yang G, Wan Y, Zhu Y, Yu M, Shen W, Wu D, Xiang Z, Genome analysis group, Yu J, Wang J, Li R, Shi J, Li H, Li G, Su J, Wang X, Li G, Zhang Z, Wu Q, Li J, Zhang Q, Wei N, Xu J, Sun H, Dong L, Liu D, Zhao S, Zhao X, Meng Q, Lan F, Huang X, Li Y, Fang L, Li C, Li D, Sun Y, Zhang Z, Yang Z, Huang Y, Xi Y, Qi Q, He D, Huang H, Zhang X, Wang Z, Li W, Cao Y, Yu Y, Yu H, Li J, Ye J, Chen H, Zhou Y, Liu B, Wang J, Ye J, Ji H, Li S, Ni P, Zhang J, Zhang Y, Zheng H, Mao B, Wang W, Ye C, Li S, Wang J, Ka-Shu Wong G, Yang H. A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 2004; 306: 1937-1940.
26. Lerat E, Burlet N, Biémont C, Vieira C. Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 2011; 473: 100-109.
27. Vieira C, Lepetit D, Dumont S, Biémont C. Wake up of transposable elements following Drosophila simulans worldwide colonization. Mol Biol Evol 1999; 16: 1251-1255.
28. Vieira C, Nardon C, Arpin C, Lepetit D, Biemont C. Evolution of genome size in Drosophila: is the invaders genome being invaded by transposable elements? Mol Biol Evol 2002; 19: 1154-1161.
29. Drevinek P, Baldwin A, Lindenburg L, Joshi LT, Marchbank A, Vosahlikova S, Dowson CG, Mahenthiralingam E. Oxidative stress of Burkholderia cenocepacia induces insertion sequencemediated genomic rearrangements that interfere with macrorestriction-based genotyping. J Clin Microbiol 2010; 48: 34-40.
30. Ohtsubo Y, Genka H, Komatsu H, Nagata Y, Tsuda M. Hightemperature-induced transposition of insertion elements in burkholderia multivorans ATCC 17616. Appl Environ Microbiol 2005; 71: 1822-1828.
31. Twiss E, Coros AM, Tavakoli NP, Derbyshire KM. Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol Microbiol 2005; 56: 1593-1607.
32. Coros CJ, Piazza CL, Chalamcharla VR, Smith D, Belfort M. Global regulators orchestrate group II intron retromobility. Mol Cell 2009; 34: 250-256.
33. Pasternak C, Ton-Hoang B, Coste G, Bailone A, Chandler M, Sommer S. Irradiation-induced Deinococcus radiodurans genome fragmentation triggers transposition of a single resident insertion sequence. PLoS Genet 2010; 6: e1000799.
34. Maumus F, Allen AE, Mhiri C, Hu H, Jabbari K, Vardi A, Grandbastien M-A, Bowler C. Potential impact of stress activated retrotransposons on genome evolution in a marine diatom. BMC Genomics 2009; 10: 624.
35. Todeschini AL, Morillon A, Springer M, Lesage P. Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 2005; 25: 7459-7472.
36. Ogasawara H, Obata H, Hata Y, Takahashi S, Gomi K. Crawler, a novel Tc1/mariner-type transposable element in Aspergillus oryzae transposes under stress conditions. Fungal Genet Biol 2009; 46: 441-449.
37. Farkash EA, Luning Prak ET. DNA damage and L1 retrotransposition. J Biomed Biotechnol 2006; 2006: 1-8.
38. Arnault C, Biémont C. Heat shocks do not mobilize mobile elements in genomes of Drosophila melanogaster inbred lines. J Mol Evol 1989; 28: 388-390.
39. Arnault C, Dufournel I. Genome and stresses: reactions against aggressions, behavior of transposable elements. Genetica 1994; 93: 149-160.
40. Vázquez JF, Albornoz J, Domínguez A. Direct determination of the effects of genotype and extreme temperature on the transposition of roo in long-term mutation accumulation lines of Drosophila melanogaster. Mol Genet Genomics 2007; 278: 653-664.
41. Rebollo R, Horard B, Hubert B, Vieira C. Jumping genes and epigenetics: towards new species. Gene 2010; 454: 1-7.
42. Menees TM, Sandmeyer SB. Cellular stress inhibits transposition of the yeast retrovirus-like element Ty3 by a ubiquitindependent block of virus-like particle formation. Proc Natl Acad Sci USA 1996; 93: 5629-5634.
43. Wardle SJ, OCarroll M, Derbyshire KM, Haniford DB. The global regulator H-NS acts directly on the transpososome to promote Tn10 transposition. Genes Dev 2005; 19: 2224-2235.
44. Whitfield CR, Wardle SJ, Haniford DB. The global bacterial regulator H-NS promotes transpososome formation and transposition in the Tn5 system. Nucleic Acids Res 2009; 37: 309-321.
45. Phalke S, Nickel O, Walluscheck D, Hortig F, Onorati MC, Reuter G. Retrotransposon silencing and telomere integrity in somatic cells of Drosophila depends on the cytosine-5 methyltransferase DNMT2. Nat Genet 2009; 41: 696-702.
46. Salzberg A, Fisher O, Siman-Tov R, Ankri S. Identification of methylated sequences in genomic DNA of adult Drosophila melanogaster. Biochem Biophys Res Commun 2004; 322: 465-469.
47. Schaefer M, Lyko F. Lack of evidence for DNA methylation of Invader4 retroelements in Drosophila and implications for Dnmt2-mediated epigenetic regulation. Nat Genet 2010; 42: 920-921.
48. Massicotte R, Whitelaw E, Angers B. DNA methylation: A source of random variation in natural populations. Epigenetics 2011; 6: 421-427.
49. Vaughn MW, Tanurd Ic M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A, Colot V, Doerge RW, Martienssen RA. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol 2007; 5: e174.
50. Turner BM. Environmental sensing by chromatin: an epigenetic contribution to evolutionary change. FEBS Lett 2011; 585: 2032-2040.
51. Hung MS, Karthikeyan N, Huang B, Koo HC, Kiger J, Shen CJ. Drosophila proteins related to vertebrate DNA (5-cytosine) methyltransferases. Proc Natl Acad Sci USA 1999; 96: 11940-11945.
52. Tweedie S, Ng HH, Barlow AL, Turner BM, Hendrich B, Bird A. Vestiges of a DNA methylation system in Drosophila melanogaster? Nat Genet 1999; 23: 389-390.
53. Krauss V, Eisenhardt C, Unger T. The genome of the stick insect Medauroidea extradentata is strongly methylated within genes and repetitive DNA. PLoS ONE 2009; 4: e7223.
54. Mandrioli M, Volpi N. The genome of the lepidopteran Mamestra brassicae has a vertebrate-like content of methyl-cytosine. Genetica 2003; 119: 187-191.
55. Field LM, Lyko F, Mandrioli M, Prantera G. DNA methylation in insects. Insect Mol Biol 2004; 13: 109-115.
56. Mandrioli M, Borsatti F. Analysis of heterochromatic epigenetic markers in the holocentric chromosomes of the aphid Acyrthosiphon pisum. Chromosome Res 2007; 15: 1015-1022.
57. Pélisson A, Sarot E, Payen-Groschêne G, Bucheton A. A novel repeat-associated small interfering RNA-mediated silencing pathway downregulates complementary sense gypsy transcripts in somatic cells of the Drosophila ovary. J Virol 2007; 81: 1951-1960.
58. Chambeyron S, Popkova A, Payen-Groschêne G, Brun C, Laouini D, Pelisson A, Bucheton A. piRNA-mediated nuclear accumulation of retrotransposon transcripts in the Drosophila female germline. Proc Natl Acad Sci USA 2008; 105: 14964-14969.
59. Kalinich JF, Catravas GN, Snyder SL. The effect of gamma radiation on DNA methylation. Radiat Res 1989; 117: 185-197.
60. Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 2004; 121: 472-480.
61. Fratelli M, Goodwin LO, Orom UA, Lombardi S, Tonelli R, Mengozzi M, Ghezzi P. Gene expression profiling reveals a signaling role of glutathione in redox regulation. Proc Natl Acad Sci USA 2005; 102: 13998-14003.
62. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 2009; 179: 572-578.
63. Servant G, Pennetier C, Lesage P. Remodeling yeast gene transcription by activating the Ty1 long terminal repeat retrotransposon under severe adenine deficiency. Mol Cell Biol 2008; 28: 5543-5554.
64. Wang H, Chai Y, Chu X, Zhao Y, Wu Y, Zhao J, Ngezahayo F, Xu C, Liu B. Molecular characterization of a rice mutatorphenotype derived from an incompatible cross-pollination reveals transgenerational mobilization of multiple transposable elements and extensive epigenetic instability. BMC Plant Biol 2009; 9: 63.
65. Brown JD, Golden D, ONeill RJ. Methylation perturbations in retroelements within the genome of a Mus interspecific hybrid correlate with double minute chromosome formation. Genomics 2008; 91: 267-273.
66. Metcalfe CJ, Bulazel KV, Ferreri GC, Schroeder-Reiter E, Wanner G, Rens W, Obergfell C, Eldridge MDB, ONeill RJ. Genomic instability within centromeres of interspecific marsupial hybrids. Genetics 2007; 177: 2507-2517.
67. ONeill RJ, ONeill MJ, Graves JA. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 1998 393: 68-72.
68. Dobigny G, Waters PD, Robinson TJ. Absence of hypomethylation and LINE-1 amplification in a white x black rhinoceros hybrid. Genetica 2006; 127: 81-86.
69. Brookfield JFY. Evolution and evolvability: celebrating Darwin Biol Lett 2009; 5: 44-46.
70. Folse HJ, Roughgarden J. What is an individual organism? A multilevel selection perspective. Q Rev Biol 2010; 85: 447-472.
71. Pavlicev M, Cheverud JM, Wagner GP. Evolution of adaptive phenotypic variation patterns by direct selection for evolvability. Proc Biol Sci 2011; 278: 1903-1912.
72. Galhardo RS, Hastings PJ, Rosenberg SM. Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 2007; 42: 399-435.
73. Chung H, Bogwitz MR, McCart C, Andrianopoulos A, Ffrench-Constant RH, Batterham P, Daborn PJ. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 2007; 175: 1071-1077.
74. Naito K, Zhang F, Tsukiyama T, Saito H, Hancock CN, Richardson AO, Okumoto Y, Tanisaka T, Wessler S.R. Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 2009; 461: 1130-1134.
75. Shilova VY, Garbuz DG, Myasyankina EN, Chen B, Evgenev MB, Feder ME, Zatsepina OG. Remarkable site specificity of local transposition into the Hsp70 promoter of Drosophila melanogaster. Genetics 2006; 173: 809-820.
76. Lerman DN, Feder ME. Naturally occurring transposable elements disrupt hsp70 promoter function in Drosophila melanogaster. Mol Biol Evol 2005; 22: 776-783.
77. Lerman DN, Michalak P, Helin AB, Bettencourt BR, Feder ME. Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol Biol Evol 2003; 20: 135-144.
78. Suprunova T, Krugman T, Distelfeld A, Fahima T, Nevo E, Korol A. Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley. Plant Mol Biol 2007; 64: 17-34.
79. Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell 2010; 40: 253-266.
80. Specchia V, Piacentini L, Tritto P, Fanti L, DAlessandro R, Palumbo G, Pimpinelli S, Bozzetti MP. Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 2010; 463: 662-665.
81. Gangaraju VK, Yin H, Weiner MM, Wang J, Huang XA, Lin H. Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat Genet 2011; 43: 153-158.
82. Pósfai G, Plunkett G, Fehér T, Frisch D, Keil GM, Umenhoffer K, Kolisnychenko V, Stahl B, Sharma SS, de Arruda M, Burland V, Harcum SW, Blattner FR. Emergent properties of reduced-genome Escherichia coli. Science 2006; 312: 1044-1046.
83. Umenhoffer K, Fehér T, Balikó G, Ayaydin F, Pósfai J, Blattner FR, Pósfai G. Reduced evolvability of Escherichia coli MDS42, an IS-less cellular chassis for molecular and synthetic biology applications. Microb Cell Fact 2010; 9: 38.
84. Paulsen IT, Banerjei L, Myers GSA, Nelson KE, Seshadri R, Read TD, Fouts D.E., Eisen JA, Gill S.R., Heidelberg JF, Tettelin H, Dodson RJ, Umayam L, Brinkac L, Beanan M, Daugherty S, DeBoy RT, Durkin S, Kolonay J, Madupu R, Nelson W, Vamathevan J, Tran B, Upton J, Hansen T, Shetty J, Khouri H, Utterback T, Radune D, Ketchum KA, Dougherty BA, Fraser CM. Role of mobile DNA in the evolution of vancomycinresistant Enterococcus faecalis. Science 2003; 299: 2071-2074.