The Foldback-like transposon Galileo is involved in the generation of two different natural chromosomal inversions of Drosophila buzzatii

Molecular Biology and Evolution

Volumn 20, Issue 5, 2003, Pages 674-685

  Casals, Ferran ^a   Cáceres, Mario ^a,b   Ruiz, Alfredo ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Chromosomal inversions; Drosophila buzzatii; Genome evolution; Hotspots; Inversion breakpoints; Transposable elements

Indexed keywords

DNA;

ARTICLE; CHROMOSOME 2Q; CHROMOSOME INVERSION; CONTROLLED STUDY; DROSOPHILA; GENE INSERTION; GENE REARRANGEMENT; GENOME; MOLECULAR CLONING; MOLECULAR EVOLUTION; MONOPHYLY; NONHUMAN; SEQUENCE ANALYSIS; SOUTHERN BLOTTING; TRANSPOSON;

ANIMALS; BASE SEQUENCE; BLOTTING, SOUTHERN; CHROMOSOME MAPPING; DNA PRIMERS; DNA PROBES; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; EVOLUTION, MOLECULAR; GENOMIC LIBRARY; IN SITU HYBRIDIZATION; INVERSION, CHROMOSOME; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

DROSOPHILA BUZZATII; INSERTION SEQUENCES; TRANSPOSONS;

EID: 0038370942     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msg070     Document Type: Article

References (62)

1. Adams, M. D., S. E. Celniker, and R. A. Holt et al. (192 coauthors). 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
2. Andolfatto, P., J. D. Wall, and M. Kreitman. 1999. Unusual haplotype structure at the proximal breakpoint of In(2L)t in a natural population of Drosophila melanogaster. Genetics 153:1297-1311.
3. Bartolomé, C., X. Maside, and B. Charlesworth. 2002. On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol. Biol. Evol. 19:926-937.
4. Berg, D. E., and M. M. Howe. 1989. Mobile DNA. American Society for Microbiology, Washington, D.C.
5. Bingham, P. M., and Z. Zachar. 1989. Retrotransposons and the FB transposon from Drosophila melanogaster. Pp. 485-502 in D. E. Berg and M. M. Howe, eds. Mobile DNA. American Society for Microbiology, Washington, D.C.
6. Brierley, H. L., and S. S. Potter. 1985. Distinct characteristics of loop sequences of two Drosophila foldback transposable elements. Nucleic Acids Res. 13:485-500.
7. Cáceres, M. 2000. Inversiones cromos6micas en Drosophila: origen molecular y significado evolutivo de su tamafio. Ph.D. thesis, Universitat Autònoma de Barcelona, Bellaterra (Barcelona), Spain.
8. Cáceres, M., M. Puig, and A. Ruiz. 2001. Molecular characterization of two natural hotspots in the Drosophila genome induced by transposon insertions. Genome Res. 11:1353-1364.
9. Cáceres, M., J. M. Ranz, A. Barbadilla, M. Long, and A. Ruiz. 1999. Generation of a widespread Drosophila inversion by a transposable element. Science 285:415-418.
10. Calvi, B. R., T. J. Hong, S. D. Findley, and W. M. Gelbart. 1991. Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. Cell 66:465-471.
11. Charlesworth, B., P. Sniegowski, and W. Stephan. 1994. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-220.
12. Cirera, S., J. M. Martín-Campos, C. Segarra, and M. Aguadé. 1995. Molecular characterization of the breakpoints of an inversion fixed between Drosophila melanogaster and D. subobscura. Genetics 139:321-326.
13. Collins, M., and G. M. Rubin. 1983. High-frequency precise excision of the Drosophila foldback transposable element. Nature 303:259-260.
14. -. 1984. Structure of chromosomal rearrangements induced by the FB transposable element in Drosophila. Nature 308:323-327.
15. Daveran-Mingot, M.-L., N. Campo, P. Ritzenthaler, and P. le Bourgeois. 1998. A natural large chromosomal inversion in Lactococcus lactis is mediated by homologous recombination between two insertion sequences. J. Bacteriol. 180:4834-4842.
16. Eanes, W. F., C. Wesley, and B. Charlesworth. 1992. Accumulation of P elements in minority inversions in natural populations of Drosophila melanogaster. Genet. Res. 59:1-9.
17. Evgen'ev, M. B., H. Zelentsova, H. Poluectova, G. T. Lyozin, V. Veleikodvorskaja, K. I. Pyatkov, L. A. Zhivotovsky, and M. G. Kidwell. 2000. Mobile elements and chromosomal evolution in the virilis group of Drosophila. Proc. Natl. Acad. Sci. USA 97:11337-11342.
18. Finnegan, D. J. 1989. Eukaryotic transposable elements and genome evolution. Trends Genet. 5:103-107.
19. Fu, Y.-X., and W.-H. Li. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
20. González, J., J. M. Ranz, and A. Ruiz. 2002. Chromosomal elements evolve at different rates in the Drosophila genome. Genetics 161:1137-1154.
21. Gray, Y. H. M. 2000. It takes two transposons to tango. Transposable-element mediated chromosomal rearrangements. Trends Genet. 16:461-468.
22. Grosshans, J., F. Schnorrer, and C. Nusslein-Volhard. 1999. Oligomerisation of tube and pelle leads to nuclear localisation of dorsal. Mech. Dev. 81:127-138.
23. Harden, N., and M. Ashburner. 1990. Characterization of the FOB-NOF transposable element of Drosophila melanogaster. Genetics 126:387-400.
24. Hasson, E., and W. F. Eanes. 1996. Contrasting histories of three gene regions associated with In(3L)Payne of Drosophila melanogaster. Genetics 144:1565-1575.
25. Hasson, E., C. Rodríguez, J. J. Fanara, H. Naveira, O. A. Reig, and A. Fontdevila. 1995. The evolutionary history of Drosophila buzzatii. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations. J. Evol. Biol. 8:369-384.
26. Heino, T. I., A. O. Saura, and V. Sorsa. 1994. Maps of the salivary gland chromosomes of Drosophila melanogaster. Dros. Inform. Serv. 73:621-738.
27. Hughes, J. F., and J. M. Coffin. 2001. Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat. Genet. 29:487-489.
28. Kim, J. M., S. Vanguri, J. D. Boeke, A. Gabriel, and D. F. Voytas. 1998. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 8:464-478.
29. Kreitman, M., and R. R. Hudson. 1991. Inferring the evolutionary histories of the Adh and Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127:565-582.
30. Krimbas, C. B., and J. R. Powell. 1992. Drosophila inversion polymorphism. CRC Press, Boca Raton, Fla.
31. Lefevre, G. Jr. 1976. A photoghraphyc representation and interpretation of the polytene chromosomes of Drosophila melanogaster salivary glands. Pp. 31-36 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Academic Press, London.
32. c Drosophila mutations. Cell 30:551-565.
33. Lim, J. K., and M. J. Simmons. 1994. Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. Bioessays 16:269-275.
34. Lobachev, K. S., B. M. Shor, H. T. Tran, W. Taylor, J. D. Keen, M. A. Resnick, and D. A. Gordenin. 1998. Factors affecting inverted repeat stimulation of recombination and deletion in Saccharomyces cerevisiae. 1998. Genetics 148:1507-1524.
35. Lyttle, T. W., and D. S. Haymer. 1992. The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster. Genetica 86:113-126.
36. Mathiopoulos, K. D., A. della Torre, V. Predazzi, V. Petrarca, and M. Coluzzi. 1998. Cloning of inversion breakpoints in the Anopheles gambiae complex traces a transposable element at the inversion junction. Proc. Natl. Acad. Sci. USA 95:12444-12449.
37. McDonald, J. F. 1993. Evolution and consequences of transposable elements. Curr. Opin. Genet. Dev. 3:855-864.
38. Montgomery, E., B. Charlesworth, and C. H. Langley. 1987. A test for role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet. Res. 49:31-41.
39. Nei, M. 1987. Molecular evolutionary genetics. Columbia University Press, New York.
40. Petes, T. D., and C. W. Hill. 1988. Recombination between repeated genes in microorganisms. Annu. Rev. Genet. 22:147-168.
41. Powell, J. R. 1997. Progress and prospects in evolutionary biology: the Drosophila model. Oxford University Press, New York.
42. Ranz, J. M., F. Casals, and A. Ruiz. 2001. How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Res. 11:230-239.
43. Regner, L. P., M. S. O. Pereira, C. E. V. Alonso, E. Abdelhay, and V. L. S. Valente. 1996. Genomic distribution of P elements in Drosophila willistoni and a search for their relationship with chromosomal inversions. J. Hered. 87:191-198.
44. Rizzon, C., G. Marais, M. Gouy, and C. Biemont. 2002. Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res. 12:400-407.
45. Rodríguez-Trelles, F., L. Alarcón, and A. Fontdevila. 2000. Molecular evolution of the buzzatii complex (Drosophila repleta group): a maximum-likelihood approach. Mol. Biol. Evol. 17:1112-1122.
46. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
47. Rozas, J., C. Segarra, G. Ribó, and M. Aguadé. 1999. Molecular population genetics of the rp49 gene region in different chromosomal inversions of Drosophila subobscura. Genetics 151:189-202.
48. Ruiz, A., and M. Wasserman. 1993. Evolutionary cytogenetics of the Drosophila buzzatii species complex. Heredity 70:582-596.
49. Russo, C.A.M., N. Takezaki, and M. Nei. 1995. Molecular phylogeny and divergence times of drosophilid species. Mol. Biol. Evol. 4:406-425.
50. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning, a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
51. Schwartz, A., D. C. Chan, L. G. Brown, R. Alagappan, D. Pettay, C. Disteche, B. McGillivray, A. de la Chapelle, and D. C. Page. 1998. Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE-LINE recombination. Hum. Mol. Genet. 7:1-11.
52. Segarra, C., E. R. Lozovskaya, G. Ribó, M. Agaudé, and D. L. Hartl. 1995. P1 clones from Drosophila melanogaster as markers to study the chromosomal evolution of Muller's A element in two species of the obscura group of Drosophila. Chromosoma 104:129-136.
53. Smith, P. A., and V. G. Corces. 1991. Drosophila transposable elements: mechanisms of mutagenesis and interactions with the host genome. Adv. Genet. 29:229-300.
54. Sniegowski, P. D., and B. Charlesworth. 1994. Transposable element numbers in cosmopolitan inversions from a natural population of Drosophila melanogaster. Genetics 137:815-827.
55. Sperlich, D., and P. Pfriem. 1986. Chromosomal polymorphism in natural and experimental populations. Pp. 257-309 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Vol. 3. Academic Press, London.
56. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
57. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
58. Truett, M. A., R. S. Jones, and S. S. Potter. 1981. Unusual structure of the FB family of transposable elements in Drosophila. Cell 24:753-763.
59. Virgin, J. B., and, J. P. Bailey. 1998. The M26 hotspot of Schizosaccharomyces pombe stimulates meiotic ectopic recombination and chromosomal rearrangements. Genetics 149:1191-1204.
60. Wesley, C. S., and W. F. Eanes. 1994. Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L) Payne in Drosophila melanogaster. Evolution 91:3132-3136.
61. Zelentsova, H., H. Poluectova, L. Mnjoian, G. Lyozin, V. Veleikodvorskaja, L. Zhivotovsky, M. G. Kidwell, and M. B. Evgen'ev. 1999. Distribution and evolution of mobile elements in the virilis species group of Drosophila. Chromosoma 108:443-56.
62. Zhou, Z-H., E. Akgün, and M. Jasin. 2001. Repeat expansion by homologous recombination in the mouse germ line at palindromic sequences. Proc. Natl. Acad. Sci USA 98:8326-8333.