Tempo and Mode of Transposable Element Activity in Drosophila
Transposable elements (TE) are stretches of DNA that propagate autonomously within genomes, but it is not clear whether TEs are moving at a constant rate or if TE activity is variable. Determining the genome-wide TE content of two closely related Drosophila species, we show that transposition rate heterogeneity is abundant. Since TE insertions are frequently associated with a selective advantage, we suggest that the observed high TE activity may have served a central role facilitating the adaptation of the two species to their novel environments after the recent out of Africa habitat expansion.
Vyšlo v časopise:
Tempo and Mode of Transposable Element Activity in Drosophila. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005406
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Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005406
Souhrn
Transposable elements (TE) are stretches of DNA that propagate autonomously within genomes, but it is not clear whether TEs are moving at a constant rate or if TE activity is variable. Determining the genome-wide TE content of two closely related Drosophila species, we show that transposition rate heterogeneity is abundant. Since TE insertions are frequently associated with a selective advantage, we suggest that the observed high TE activity may have served a central role facilitating the adaptation of the two species to their novel environments after the recent out of Africa habitat expansion.
Zdroje
1. Charlesworth B, Charlesworth D. The population dynamics of transposable elements. Genetical Research. 1983;42(01):1–27.
2. Petrov DA, Fiston-Lavier AS, Lipatov M, Lenkov K, González J. Population genomics of transposable elements in Drosophila melanogaster. Molecular biology and evolution. 2011;28(5):1633–44. doi: 10.1093/molbev/msq337 21172826
3. Barrón MG, Fiston-Lavier AS, Petrov DA, González J. Population Genomics of Transposable Elements in Drosophila. Annual review of genetics. 2014;48:561–581. doi: 10.1146/annurev-genet-120213-092359 25292358
4. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE. Size matters: non-LTR retrotransposable elements and ectopic recombination in Drosophila. Molecular biology and evolution. 2003;20(6):880–92. doi: 10.1093/molbev/msg102 12716993
5. Kofler R, Betancourt AJ, Schlötterer C. Sequencing of Pooled DNA Samples (Pool-Seq) Uncovers Complex Dynamics of Transposable Element Insertions in Drosophila melanogaster. PLoS genetics. 2012;8(1):e1002487. doi: 10.1371/journal.pgen.1002487 22291611
6. Bergman CM, Bensasson D. Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America. 2007 Jul;104(27):11340–5. doi: 10.1073/pnas.0702552104 17592135
7. Charlesworth B, Langley CH. The population genetics of Drosophila transposable elements. Annual review of genetics. 1989;23:251–87. doi: 10.1146/annurev.ge.23.120189.001343 2559652
8. Eickbush DG, Eickbush TH. Vertical transmission of the retrotransposable elements R1 and R2 during the evolution of the Drosophila melanogaster species subgroup. Genetics. 1995;139(2):671–684. 7713424
9. Malik HS, Burke WD, Eickbush TH. The age and evolution of non-LTR retrotransposable elements. Molecular Biology and Evolution. 1999;16(6):793–805. doi: 10.1093/oxfordjournals.molbev.a026164 10368957
10. Nuzhdin SV. Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica. 1999;107(1–3):129–137. doi: 10.1023/A:1003957323876 10952206
11. Nuzhdin SV, Pasyukova EG, Morozova EA, Flavell AJ. Quantitative genetic analysis of copia retrotransposon activity in inbred Drosophila melanogaster lines. Genetics. 1998;150(2):755–766. 9755206
12. Lohe AR, Moriyama EN, Lidholm DA, Hartl DL. Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Molecular biology and evolution. 1995;12(1):62–72. doi: 10.1093/oxfordjournals.molbev.a040191 7877497
13. Burt A, Trivers R. Genes in conflict: the biology of selfish genetic elements. Belknap Press; 2008.
14. Silva JC, Loreto EL, Clark JB. Factors that affect the horizontal transfer of transposable elements. Current issues in molecular biology. 2004;6:57–71. 14632259
15. Lachaise D, Cariou ML, David JR, Lemeunier F. Historical biogeography of the Drosophila melanogaster species subgroup. Evolutionary Biology. 1988;22:159–222.
16. Hey J, Kliman RM. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Molecular Biology and Evolution. 1993;p. 804–822. 8355601
17. Palmieri N, Nolte V, Chen J, Schlötterer C. Assembly and annotation of Drosophila simulans strains from Madagascar. Genome resources. 2014;.
18. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW, et al. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS biology. 2007;5(11):e310. doi: 10.1371/journal.pbio.0050310 17988176
19. Hu TT, Eisen MB, Thornton KR, Andolfatto P. A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome research. 2013;23(1):89–98. doi: 10.1101/gr.141689.112 22936249
20. Schlötterer C, Tobler R, Kofler R, Nolte V. Sequencing pools of individuals mining genome-wide polymorphism data without big funding. Nature Reviews Genetics. 2014;advance on. 25246196
21. Quesneville H, Bergman CM, Andrieu O, Autard D, Nouaud D, Ashburner M, et al. Combined evidence annotation of transposable elements in genome sequences. PLoS computational biology. 2005;1(2):166–75. doi: 10.1371/journal.pcbi.0010022 16110336
22. Kaminker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, et al. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome biology. 2002;3(12). doi: 10.1186/gb-2002-3-12-research0084
23. Zhuang J, Wang J, Theurkauf W, Weng Z. TEMP: a computational method for analyzing transposable element polymorphism in populations. Nucleic acids research. 2014;. doi: 10.1093/nar/gku323
24. Kofler R, Hill T, Nolte V, Betancourt A, Schlötterer C. The recent invasion of natural Drosophila simulans populations by the P-element. Proceedings of the National Academy of Sciences. 2015;. doi: 10.1073/pnas.1500758112
25. Kapitonov VV, Jurka J. Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(11):6569–74. doi: 10.1073/pnas.0732024100 12743378
26. Singh ND, Petrov DA. Rapid sequence turnover at an intergenic locus in Drosophila. Molecular biology and evolution. 2004;21(4):670–80. doi: 10.1093/molbev/msh060 14739245
27. Dowsett AP, Young MW. Differing levels of dispersed repetitive DNA among closely related species of Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 1982 Aug;79(15):4570–4. doi: 10.1073/pnas.79.15.4570 6956880
28. 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(4):875–88. 2900794
29. Vieira C, Lepetit D, Dumont S, Biémont C. Wake up of transposable elements following Drosophila simulans worldwide colonization. Molecular biology and evolution. 1999;16(9):1251–5. doi: 10.1093/oxfordjournals.molbev.a026215 10486980
30. Charlesworth, B, Sniegowski, P, Stephan, W. The evolutionary dynamics of repetitive DNA in eukaryotes. 1994;.
31. Charlesworth B, Lapid A, et al. The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. I. Element frequencies and distribution. Genetical research. 1992;60(02):103–114. doi: 10.1017/S0016672300030792 1334899
32. Maumus F, Fiston-Lavier AS, Quesneville H. Impact of transposable elements on insect genomes and biology. Current Opinion in Insect Science. 2015;.
33. Brookfield JF, Montgomery E, Langley CH. Apparent absence of transposable elements related to the P elements of D. melanogaster in other species of Drosophila. Nature. 1982;310(5975):330–2. doi: 10.1038/310330a0
34. Engels WR. The origin of P elements in Drosophila melanogaster. BioEssays. 1992;14(10):681–6. doi: 10.1002/bies.950141007 1285420
35. Lockton S, Ross-Ibarra J, Gaut BS. Demography and weak selection drive patterns of transposable element diversity in natural populations of Arabidopsis lyrata. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(37):13965–70. doi: 10.1073/pnas.0804671105 18772373
36. Lynch M, Conery JS. The origins of genome complexity. Science (New York, NY). 2003;302(5649):1401–4. doi: 10.1126/science.1089370
37. Nolte V, Schlötterer C. African Drosophila melanogaster and D. simulans populations have similar levels of sequence. Genetics. 2008;178(1):405–12. doi: 10.1534/genetics.107.080200 18202383
38. True JR, Mercer JM, Laurie CC. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996;142(2):507–523. 8852849
39. Biémont C, Nardon C, Deceliere G, Lepetit D. Worldwide distribution of transposable element copy number in natural populations of Drosophila simulans. Evolution. 2003;57(1):159–167. doi: 10.1554/0014-3820(2003)057%5B0159:WDOTEC%5D2.0.CO;2 12643577
40. Caracristi G, Schlötterer C. Genetic differentiation between American and European Drosophila melanogaster populations could be attributed to admixture of African alleles. Molecular biology and evolution. 2003;20(5):792–9. doi: 10.1093/molbev/msg091 12679536
41. Nunes MD, Neumeier H, Schlötterer C. Contrasting patterns of natural variation in global Drosophila melanogaster populations. Molecular ecology. 2008;17(20):4470–4479. doi: 10.1111/j.1365-294X.2008.03944.x 18986493
42. Blumenstiel JP, Hartl DL, Lozovsky ER. Patterns of insertion and deletion in contrasting chromatin domains. Molecular biology and evolution. 2002;19(12):2211–25. doi: 10.1093/oxfordjournals.molbev.a004045 12446812
43. Blumenstiel JP, Chen X, He M, Bergman CM. An Age-of-Allele Test of Neutrality for Transposable Element Insertions. Genetics. 2013;196:523–38. doi: 10.1534/genetics.113.158147 24336751
44. Kidwell MG. Evolution of hybrid dysgenesis determinants in Drosophila melanogaster. Proceedings of the National Academy of Sciences. 1983;80(6):1655–1659. doi: 10.1073/pnas.80.6.1655
45. Bowen NJ, McDonald JF. Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome research. 2001;11(9):1527–1540. doi: 10.1101/gr.164201 11544196
46. Bartolomé C, Bello X, Maside X. Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome biology. 2009;10(2):R22. doi: 10.1186/gb-2009-10-2-r22 19226459
47. Sturtevant AH. A Case of Rearrangement of Genes in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 1921;7(8):235–7. doi: 10.1073/pnas.7.8.235 16576597
48. Lerat E, Burlet N, Biémont C, Vieira C. Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene. 2011;473(2):100–109. doi: 10.1016/j.gene.2010.11.009 21156200
49. Vieira C, Biémont C. Transposable Element Dynamics in Two Sibling Species: Drosophila melanogaster and Drosophila simulans. Genetica. 2004;120(1–3):115–123. doi: 10.1023/B:GENE.0000017635.34955.b5 15088652
50. Vieira C, Fablet M, Lerat E, Boulesteix M, Rebollo R, Burlet N, et al. A comparative analysis of the amounts and dynamics of transposable elements in natural populations of Drosophila melanogaster and Drosophila simulans. Journal of environmental radioactivity. 2012;113:83–86. doi: 10.1016/j.jenvrad.2012.04.001 22659421
51. Plasterk RH, Izsvák Z, Ivics Z. Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends in genetics: TIG. 1999;15(8):326–32. doi: 10.1016/S0168-9525(99)01777-1 10431195
52. Anxolabéhère D, Kidwell MG, Periquet G. Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. Molecular biology and evolution. 1988;5(3):252–69. 2838720
53. Khurana JS, Wang J, Xu J, Koppetsch BS, Thomson TC, Nowosielska A, et al. Adaptation to P element transposon invasion in Drosophila melanogaster. Cell. 2011;147(7):1551–63. doi: 10.1016/j.cell.2011.11.042 22196730
54. Petrov DA, Schutzman JL, Hartl DL, Lozovskaya ER. Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proceedings of the National Academy of Sciences of the United States of America. 1995;92(17):8050–4. doi: 10.1073/pnas.92.17.8050 7644536
55. McClintock B. The significance of responses of the genome to challenge. Science (New York, NY). 1984;226(4676):792–801. doi: 10.1126/science.15739260
56. Bucheton A, Vaury C, Chaboissier MC, Abad P, Pélisson A, Simonelig M. I elements and the Drosophila genome. Genetica. 1992;86(1–3):175–90. doi: 10.1007/BF00133719 1281801
57. Sánchez-Gracia A, Maside X, Charlesworth B. High rate of horizontal transfer of transposable elements in Drosophila. Trends in genetics: TIG. 2005;21(4):200–3. doi: 10.1016/j.tig.2005.02.001 15797612
58. Casacuberta E, González J. The impact of transposable elements in environmental adaptation. Molecular ecology. 2013;22(6):1503–17. doi: 10.1111/mec.12170 23293987
59. Gonzalez J, Petrov DA. Evolution of genome content: population dynamics of transposable elements in flies and humans. In: Evolutionary Genomics. Springer; 2012. p. 361–383.
60. Dolgin ES, Charlesworth B. The effects of recombination rate on the distribution and abundance of transposable elements. Genetics. 2008;178(4):2169–2177. doi: 10.1534/genetics.107.082743 18430942
61. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. Bursts of retrotransposition reproduced in Arabidopsis. Nature. 2009;461(7262):423–426. doi: 10.1038/nature08351 19734880
62. Wright SI, Schoen DJ. Transposon dynamics and the breeding system. Genetica. 1999;107(1–3):139–148. doi: 10.1023/A:1003953126700 10952207
63. Fiston-Lavier AS, Singh ND, Lipatov M, Petrov DA. Drosophila melanogaster recombination rate calculator. Gene. 2010;463(1–2):18–20. doi: 10.1016/j.gene.2010.04.015 20452408
64. Schaack S, Gilbert C, Feschotte C. Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends in ecology & evolution. 2010;25(9):537–46. doi: 10.1016/j.tree.2010.06.001
65. Capy P, Gibert P. Drosophila melanogaster, Drosophila simulans: so similar yet so different. Genetica. 2004;120(1–3):5–16. doi: 10.1023/B:GENE.0000017626.41548.97 15088643
66. Stephan W, Li H. The recent demographic and adaptive history of Drosophila melanogaster. Heredity. 2007;98(2):65–8. doi: 10.1038/sj.hdy.6800901 17006533
67. Levin HL, Moran JV. Dynamic interactions between transposable elements and their hosts. Nature reviews Genetics. 2011;12(9):615–27. doi: 10.1038/nrg3030 21850042
68. McCoy RC, Taylor RW, Blauwkamp TA, Kelley JL, Kertesz M, Pushkarev D, et al. Illumina TruSeq Synthetic Long-Reads Empower De Novo Assembly and Resolve Complex, Highly-Repetitive Transposable Elements. PLoS ONE. 2014;9(9):e106689. doi: 10.1371/journal.pone.0106689 25188499
69. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic acids research. 1988;16(3):1215. doi: 10.1093/nar/16.3.1215 3344216
70. Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0; 1996–2010. Available from: http://www.repeatmasker.org.
71. Permal E, Flutre T, Quesneville H. Roadmap for annotating transposable elements in eukaryote genomes. Methods in molecular biology (Clifton, NJ). 2012;859:53–68. doi: 10.1007/978-1-61779-603-6_3
72. Kofler R, Schlötterer C, Lelley T. SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics (Oxford, England). 2007;23(13):1683–5. doi: 10.1093/bioinformatics/btm157
73. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics (Oxford, England). 2010;26(6):841–842. doi: 10.1093/bioinformatics/btq033
74. Li H, Durbin R. Fast and accurate short read alignment with Burrows Wheeler transform. Bioinformatics. 2009;25(14):1754–1760. doi: 10.1093/bioinformatics/btp324 19451168
75. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England). 2010;26(5):589–95. doi: 10.1093/bioinformatics/btp698
76. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, Futschik A, et al. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PloS one. 2011;6(1):e15925. doi: 10.1371/journal.pone.0015925 21253599
77. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England). 2009 Aug;25(16):2078–9. doi: 10.1093/bioinformatics/btp352
78. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome biology. 2004;5(2):R12. doi: 10.1186/gb-2004-5-2-r12 14759262
79. Le Rouzic A, Boutin TS, Capy P. Long-term evolution of transposable elements. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(49):19375–80. doi: 10.1073/pnas.0705238104 18040048
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