A genome-wide survey of genetic instability by transposition in Drosophila hybrids

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Vela, Doris ^a,d   Fontdevila, Antonio ^a   Vieira, Cristina ^b,c   Pilar García Guerreiro, María ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITÉ LYON 1   (France)

^c INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DEL ECUADOR   (Ecuador)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PRIMER DNA; TRANSPOSON;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA TRANSPOSITION; DROSOPHILA; DROSOPHILA BUZZATII; DROSOPHILA KOEPFERAE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC MARKER; GENOME ANALYSIS; GENOMIC INSTABILITY; GENOMIC STRESS; INTERSPECIFIC HYBRID; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE ANALYSIS; RETROPOSON; STRESS; TRANSPOSON; ANIMAL; CROSS BREEDING; GENETICS; GENOMICS; HYBRIDIZATION; NONPARAMETRIC TEST; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; CROSSES, GENETIC; DNA PRIMERS; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; GENOMIC INSTABILITY; GENOMICS; HYBRIDIZATION, GENETIC; IN SITU HYBRIDIZATION, FLUORESCENCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STATISTICS, NONPARAMETRIC;

EID: 84897745655     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088992     Document Type: Article

References (62)

1. Arnold M (1997) Evolution through genetic exchange. Oxford University Press.
2. Arnold M (2006) Natural hybridization and Evolution. Oxford University Press.
3. Pollock (1988) A morphometric analysis of a Pseudopanax hybrid swarm. University of Auckland.
4. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, et al. (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science (80-) 301: 1211-1216. Available: http://www.ncbi.nlm.nih. gov/pubmed/12907807.
5. Nolte AW, Tautz D (2010) Understanding the onset of hybrid speciation. Trends Genet 26: 54-58. Available: http://linkinghub.elsevier.com/retrieve/pii/ S0168952509002492.
6. Fontdevila A (2004) Evolution: from Molecules to Ecosystems. In: Moya A, Font E, editors. Introgression and hybrid speciation via transposition. Oxford University Press. 182-194.
7. Michalak P (2010) An eruption of mobile elements in genomes of hybrid sunflowers. Heredity (Edinb) 104: 329-330. Available: http://europepmc.org/ abstract/MED/20068587.
8. Capy P, Langin T, Anxolabehere, Dominique Bazin C (1998) Dynamics and Evolution of Transposable Elements. Thomson Learning.
9. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285. Available: http://dx.doi.org/10.1038/nrg2072.
10. García Guerreiro MP (2012) What makes transposable elements move in the Drosophila genome? Heredity (Edinb) 108: 461-468. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3330689&tool= pmcentrez&rendertype=abstract. Accessed 14 October 2013.
11. Ginzburg LEVR, Bincham PM, Yoo S (1984) On the theory of speciation induced by transposable elements. Genetics 107: 331-341.
12. Ish-Horowicz D (1982) Transposable elements, hybrid incompatibility and speciation. Nature 299: 676-677. Available: http://dx.doi.org/10.1038/299676a0.
13. Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P-M hybrid dysgenesis: The nature of induced mutations. Cell 29: 987-994. Available: http://linkinghub.elsevier.com/retrieve/pii/0092867482904627.
14. Bingham PM, Kidwell MG, Rubin GM (1982) The molecular basis of P-M hybrid dysgenesis: The role of the P element, a P-strain-specific transposon family. Cell 29: 995-1004. Available: http://linkinghub.elsevier.com/retrieve/pii/ 0092867482904639.
15. Picard (1976) Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics 85: 107-123.
16. Yannopoulos G, Stamatis N, Monastirioti M, Hatzopoulos P, Louis C (1987) hobo is responsible for the induction of hybrid dysgenesis by strains of Drosophila melanogaster bearing the male recombination factor 23.5MRF. Cell 49: 487-495. Available: http://linkinghub.elsevier.com/retrieve/pii/ 009286748790451X.
17. Petrov DA, Schutzman JL, Hartl DL, Lozovskaya ER (1995) Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. Proc Natl Acad Sci U S A 92: 8050-8054. Available: http://europepmc.org/ abstract/MED/7644536.
18. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, et al. (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322: 1387-1392. Available: http://europepmc.org/abstract/MED/ 19039138.
19. Akkouche A, Grentzinger T, Fablet M, Armenise C, Burlet N, et al. (2013) Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells. EMBO Rep 14: 458-464. Available: http://www.ncbi.nlm.nih.gov/ pubmed/23559065. Accessed 4 October 2013.
20. Rebollo R, Horard B, Hubert B, Vieira C (2010) Jumping genes and epigenetics: Towards new species. Gene 454: 1-7. Available: http://www. sciencedirect.com/science/article/pii/S0378111910000296.
21. Josefsson C, Dilkes B, Comai L (2006) Parent-Dependent Loss of Gene Silencing during Interspecies Hybridization. Curr Biol 16: 1322-1328. Available: http://www.sciencedirect.com/science/article/pii/S0960982206016289.
22. Liu B, Wendel JF (2000) Retrotransposon activation followed by rapid repression in introgressed rice plants. Genome 43: 874-880. Available: http://www.nrcresearchpress.com/doi/abs/10.1139/g00-058.
23. Shan X, Liu Z, Dong Z, Wang Y, Chen Y, et al. (2005) Mobilization of the Active MITE Transposons mPing and Pong in Rice by Introgression from Wild Rice (Zizania latifolia Griseb.). Mol Biol Evol 22: 976-990. Available: http://mbe.oxfordjournals.org/content/22/4/976.abstract.
24. Ungerer MC, Strakosh SC, Zhen Y (2006) Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. 16. Available: http://dx.doi.org/10.1016/j.cub.2006.09.020.
25. Shivaprasad P V, Dunn RM, Santos BA, Bassett A, Baulcombe DC (2012) Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31: 257-266. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3261569&tool= pmcentrez&rendertype=abstract. Accessed 8 October 2013.
26. Coyne JA (1989) Mutation rates in hybrids between sibling species of Drosophila. Heredity (Edinb) 63: 155-162. Available: http://dx.doi.org/10.1038/ hdy.1989.87.
27. Hey J (1988) Speciation via hybrid dysgenesis: negative evidence from the Drosophila affinis subgroup. Genetica 78: 97-103. Available: http://dx.doi.org/10.1007/BF00058840.
28. Metcalfe CJ, Bulazel K V, Ferreri GC, Schroeder-Reiter E, Wanner G, et al. (2007) Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids. Genet 177: 2507-2517. Available: http://www.genetics.org/content/177/4/ 2507.abstract.
29. O'Neill RJW, O'Neill MJ, Graves JAM (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68-72. Available: http://dx.doi.org/10.1038/29985.
30. Labrador M, Fontdevila A (1994) High transposition rates of Osvaldo, a new Drosophila buzzatii retrotransposon. Mol Gen Genet 245: 661-674.
31. Labrador M, Farré M, Utzet F, Fontdevila a (1999) Interspecific hybridization increases transposition rates of Osvaldo. Mol Biol Evol 16: 931-937. Available: http://www.ncbi.nlm.nih.gov/pubmed/10406110.
32. Pinol J, Francino O, Fontdevila A, Cabré O (1988) Rapid isolation of Drosophila high molecular weight DNA to obtain genomic libraries. Nucleic Acids Res 16: 2736. Available: http://nar.oxfordjournals.org/content/16/6/2736. short.
33. Vela D, Guerreiro MP, Fontdevila A (2011) Adaptation of the AFLP technique as a new tool to detect genetic instability and transposition in interspecific hybrids. Biotechniques 50: 247-250. Available: http://europepmc.org/abstract/MED/21548908.
34. Zampicinini G, Blinov A, Cervella P, Guryev V, Sella G (2004) Insertional polymorphism of a non-LTR mobile element (NLRCth1) in European populations of Chironomus riparius (Diptera, Chironomidae) as detected by transposon insertion display. Genome 47: 1154-1163. Available: http://europepmc.org/abstract/MED/ 15644974.
35. Akkouche A, Rebollo R, Burlet N, Esnault C, Martinez S, et al. (2012) tirant, a Newly Discovered Active Endogenous Retrovirus in Drosophila simulans: 3675-3681. doi:10.1128/JVI.07146-11.
36. García Guerreiro MP, Fontdevila A (2007) The evolutionary history of Drosophila buzzatii. XXXVI. Molecular structural analysis of Osvaldo retrotransposon insertions in colonizing populations unveils drift effects in founder events. Genetics 175: 301-310. (Pubitemid 46168574)
37. Kruskal WH, Wallis WA (1952) Use of Ranks in One-Criterion Variance Analysis. J Am Stat Assoc 47: 583-621. Available: http://www.jstor.org/stable/ 2280779.
38. Jurka J, Kapitonov V V, Pavlicek A, Klonowski P, Kohany O, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110: 462-467. Available: http://europepmc.org/abstract/MED/16093699.
39. Vieira C, Biémont C (1996) Geographical variation in insertion site number of retrotransposon 412 in Drosophila simulans. J Mol Evol 42: 443-451. (Pubitemid 26154321)
40. Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17: 6086-6095. Available: http://dx.doi.org/10.1093/emboj/17.20.6086.
41. Pantazidis A, Labrador M, Fontdevila A (1999) The retrotransposon Osvaldo from Drosophila buzzatiidisplays all structural features of a funcrional retrovirus. Mol Biol Evol 16: 909-921. (Pubitemid 29314169)
42. Steinau AN, Skinner DZ, Steinau M (2003) Mechanism of extreme genetic recombination in weedy Amaranthus hybrids. Weed Sci 51: 696-701. Available: http://wssajournals.org/doi/abs/10.1614/P2002-159.
43. Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, et al. (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41: 221-230. Available: http://dx.doi.org/10.1111/j.1365-313X.2004.02297.x.
44. Coyne JA (1986) Meiotic segregation and male recombination in intespecific hybrids of Drosophila. Genetics 114: 485-494. Available: http://www.genetics.org/content/114/2/485.abstract.
45. Kawakami T, Strakosh SC, Zhen Y, Ungerer MC (2010) Different scales of Ty1/copia-like retrotransposon proliferation in the genomes of three diploid hybrid sunflower species. Heredity (Edinb) 104: 341-350. Available: http://dx.doi.org/10.1038/hdy.2009.182.
46. Labrador M, Farré M, Utzet F, Fontdevila A (1999) Interspecific hybridization increases transposition rates of Osvaldo. Mol Biol Evol 16: 931-937. Available: http://mbe.oxfordjournals.org/content/16/7/931.abstract.
47. Kelleher ES, Edelman NB, Barbash DA (2012) Drosophila Interspecific Hybrids Phenocopy piRNA-Pathway Mutants. PLoS Biol 10. Available: http://dx.doi.org/10.1371/journal.pbio.1001428.
48. Suh DS, Choi EH, Yamazaki T, Harada K (1995) Studies on the transposition rates of mobile genetic elements in a natural population of Drosophila melanogaster. Mol Biol Evol 12: 748-758. Available: http://mbe.oxfordjournals. org/content/12/5/748.abstract.
49. Sheen F, Lim JK, Simmons MJ (1993) Genetic instability in Drosophila melanogaster mediated by hobo transposable elements. Genet 133: 315-334. Available: http://www.genetics.org/content/133/2/315.abstract.
50. Roy MA, Carroll LM, Kass HD, Nguyen VS, Salem A-H, et al. (1999) Recently integrated human Alu repeats: finding needles in the haystack. Genetica 107: 149-161. doi:10.1023/A:1003941704138. (Pubitemid 129574961)
51. Marzo M, Puig M, Ruiz A (2008) The Foldback-like element Galileo belongs to the P superfamily of DNA transposons and is widespread within the Drosophila genus. Proc Natl Acad Sci 105: 2957-2962. Available: http://www.pnas.org/ content/105/8/2957.abstract.
52. Finnegan DJ (1992) Transposable elements. Curr Opin Genet Dev 2: 861-867. Available: http://www.sciencedirect.com/science/article/pii/S0959437X0580108X.
53. Hoskins R a, Smith CD, Carlson JW, Carvalho a B, Halpern A, et al. (2002) Heterochromatic sequences in a Drosophila whole-genome shotgun assembly. Genome Biol 3: RESEARCH0085. Available: http://www.pubmedcentral.nih.gov/ articlerender.fcgi?artid=151187&tool=pmcentrez&rendertype=abstract.
54. Labrador M, Naveira H, Fontdevila A (1990) Genetic mapping of the Adh locus in the repleta group of Drosophila by in situ hybridization. J Hered 81: 83-86. (Pubitemid 20182449)
55. Desset S, Meignin C, Dastugue B, Vaury C (2003) COM, a Heterochromatic Locus Governing the Control of Independent Endogenous Retroviruses From Drosophila melanogaster. Genet 164: 501-509. Available: http://www.genetics.org/ content/164/2/501.abstract.
56. Pélisson A, Song SU, Prud'homme N, Smith PA, Bucheton A, et al. (1994) Gypsy transposition correlates with the production of a retroviral envelope-like protein under the tissue-specific control of the Drosophila flamenco gene. EMBO J 13: 4401-4411. Available: http://europepmc.org/abstract/ MED/7925283.
57. Stuart JR, Haley KJ, Swedzinski D, Lockner S, Kocian PE, et al. (2002) Telomeric P elements associated with cytotype regulation of the P transposon family in Drosophila melanogaster. Genetics 162: 1641-1654. Available: http://europepmc.org/abstract/MED/12524339.
58. Nuzhdin S V, Mackay TF (1995) The genomic rate of transposable element movement in Drosophila melanogaster. Mol Biol Evol 12: 180-181. Available: http://europepmc.org/abstract/MED/7877494.
59. Vu W, Nuzhdin S (2011) Genetic variation of copia suppression in Drosophila melanogaster. Heredity (Edinb) 106: 207-217. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3183883&tool= pmcentrez&rendertype=abstract.Accessed 14 October 2013.
60. Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, et al. (2009) Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell 137: 522-535. Available: http://dx.doi.org/10.1016/j.cell.2009.03. 040.
61. Malone JH, Michalak P (2008) Gene expression analysis of the ovary of hybrid females of Xenopus laevis and X. muelleri. BMC Evol Biol 8: 82. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid= 2330042&tool=pmcentrez&rendertype=abstract. Accessed 14 October 2013.
62. Naveira H, Fontdevila A (1985) The evolutionary history of Drosophila buzzatii. IX. High frequencies of new chromosome rearrangements induced by introgressive hybridization. Chromosoma 91: 87-94. Available: http://europepmc.org/abstract/MED/3987443.