• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Dec 2003; 165(4): 1831–1842.
PMCID: PMC1462885

The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila.


In recombinational DNA double-strand break repair a homologous template for gene conversion may be located at several different genomic positions: on the homologous chromosome in diploid organisms, on the sister chromatid after DNA replication, or at an ectopic position. The use of the homologous chromosome in mitotic gene conversion is thought to be limited in the yeast Saccharomyces cerevisiae and mammalian cells. In contrast, by studying the repair of double-strand breaks generated by the I-SceI rare-cutting endonuclease, we find that the homologous chromosome is frequently used in Drosophila melanogaster, which we suggest is attributable to somatic pairing of homologous chromosomes in mitotic cells of Drosophila. We also find that Drosophila mitotic cells of the germ line, like yeast, employ the homologous recombinational repair pathway more often than imperfect nonhomologous end joining.

Full Text

The Full Text of this article is available as a PDF (223K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adams Melissa D, McVey Mitch, Sekelsky Jeff J. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science. 2003 Jan 10;299(5604):265–267. [PubMed]
  • Beall EL, Rio DC. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev. 1997 Aug 15;11(16):2137–2151. [PMC free article] [PubMed]
  • Bellaiche Y, Mogila V, Perrimon N. I-SceI endonuclease, a new tool for studying DNA double-strand break repair mechanisms in Drosophila. Genetics. 1999 Jul;152(3):1037–1044. [PMC free article] [PubMed]
  • Bibikova Marina, Golic Mary, Golic Kent G, Carroll Dana. Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. Genetics. 2002 Jul;161(3):1169–1175. [PMC free article] [PubMed]
  • Burgess SM, Kleckner N, Weiner BM. Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev. 1999 Jun 15;13(12):1627–1641. [PMC free article] [PubMed]
  • Colleaux L, D'Auriol L, Galibert F, Dujon B. Recognition and cleavage site of the intron-encoded omega transposase. Proc Natl Acad Sci U S A. 1988 Aug;85(16):6022–6026. [PMC free article] [PubMed]
  • Donoho G, Jasin M, Berg P. Analysis of gene targeting and intrachromosomal homologous recombination stimulated by genomic double-strand breaks in mouse embryonic stem cells. Mol Cell Biol. 1998 Jul;18(7):4070–4078. [PMC free article] [PubMed]
  • Ducau J, Bregliano JC, de La Roche Saint-André C. Gamma-irradiation stimulates homology-directed DNA double-strand break repair in Drosophila embryo. Mutat Res. 2000 Jun 30;460(1):69–80. [PubMed]
  • Engels WR, Johnson-Schlitz DM, Eggleston WB, Sved J. High-frequency P element loss in Drosophila is homolog dependent. Cell. 1990 Aug 10;62(3):515–525. [PubMed]
  • Maryon E, Carroll D. Characterization of recombination intermediates from DNA injected into Xenopus laevis oocytes: evidence for a nonconservative mechanism of homologous recombination. Mol Cell Biol. 1991 Jun;11(6):3278–3287. [PMC free article] [PubMed]
  • Engels WR, Preston CR, Johnson-Schlitz DM. Long-range cis preference in DNA homology search over the length of a Drosophila chromosome. Science. 1994 Mar 18;263(5153):1623–1625. [PubMed]
  • Esposito MS. Evidence that spontaneous mitotic recombination occurs at the two-strand stage. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4436–4440. [PMC free article] [PubMed]
  • Moynahan ME, Jasin M. Loss of heterozygosity induced by a chromosomal double-strand break. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):8988–8993. [PMC free article] [PubMed]
  • Fabre F. Induced intragenic recombination in yeast can occur during the G1 mitotic phase. Nature. 1978 Apr 27;272(5656):795–798. [PubMed]
  • Fung JC, Marshall WF, Dernburg A, Agard DA, Sedat JW. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J Cell Biol. 1998 Apr 6;141(1):5–20. [PMC free article] [PubMed]
  • Pâques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999 Jun;63(2):349–404. [PMC free article] [PubMed]
  • Gloor GB, Preston CR, Johnson-Schlitz DM, Nassif NA, Phillis RW, Benz WK, Robertson HM, Engels WR. Type I repressors of P element mobility. Genetics. 1993 Sep;135(1):81–95. [PMC free article] [PubMed]
  • Perrin A, Buckle M, Dujon B. Asymmetrical recognition and activity of the I-SceI endonuclease on its site and on intron-exon junctions. EMBO J. 1993 Jul;12(7):2939–2947. [PMC free article] [PubMed]
  • Golic MM, Golic KG. A quantitative measure of the mitotic pairing of alleles in Drosophila melanogaster and the influence of structural heterozygosity. Genetics. 1996 May;143(1):385–400. [PMC free article] [PubMed]
  • Plessis A, Perrin A, Haber JE, Dujon B. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics. 1992 Mar;130(3):451–460. [PMC free article] [PubMed]
  • Gong Wei J, Golic Kent G. Ends-out, or replacement, gene targeting in Drosophila. Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2556–2561. [PMC free article] [PubMed]
  • Hiraoka Y, Dernburg AF, Parmelee SJ, Rykowski MC, Agard DA, Sedat JW. The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J Cell Biol. 1993 Feb;120(3):591–600. [PMC free article] [PubMed]
  • Preston Christine R, Engels William, Flores Carlos. Efficient repair of DNA breaks in Drosophila: evidence for single-strand annealing and competition with other repair pathways. Genetics. 2002 Jun;161(2):711–720. [PMC free article] [PubMed]
  • Kadyk LC, Hartwell LH. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics. 1992 Oct;132(2):387–402. [PMC free article] [PubMed]
  • Puchta H, Dujon B, Hohn B. Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. Nucleic Acids Res. 1993 Nov 11;21(22):5034–5040. [PMC free article] [PubMed]
  • Jeggo PA. DNA breakage and repair. Adv Genet. 1998;38:185–218. [PubMed]
  • Richardson C, Moynahan ME, Jasin M. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 1998 Dec 15;12(24):3831–3842. [PMC free article] [PubMed]
  • Johnson RD, Jasin M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 2000 Jul 3;19(13):3398–3407. [PMC free article] [PubMed]
  • Rong YS, Golic KG. Dominant defects in Drosophila eye pigmentation resulting from a euchromatin-heterochromatin fusion gene. Genetics. 1998 Dec;150(4):1551–1566. [PMC free article] [PubMed]
  • Rong YS, Golic KG. Gene targeting by homologous recombination in Drosophila. Science. 2000 Jun 16;288(5473):2013–2018. [PubMed]
  • Lee SE, Pâques F, Sylvan J, Haber JE. Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths. Curr Biol. 1999 Jul 15;9(14):767–770. [PubMed]
  • Rong Yikang S, Titen Simon W, Xie Heng B, Golic Mary M, Bastiani Michael, Bandyopadhyay Pradip, Olivera Baldomero M, Brodsky Michael, Rubin Gerald M, Golic Kent G. Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 2002 Jun 15;16(12):1568–1581. [PMC free article] [PubMed]
  • Rouet P, Smih F, Jasin M. Expression of a site-specific endonuclease stimulates homologous recombination in mammalian cells. Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6064–6068. [PMC free article] [PubMed]
  • Liang F, Han M, Romanienko PJ, Jasin M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5172–5177. [PMC free article] [PubMed]
  • Sjögren C, Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol. 2001 Jun 26;11(12):991–995. [PubMed]
  • Stark Jeremy M, Jasin Maria. Extensive loss of heterozygosity is suppressed during homologous repair of chromosomal breaks. Mol Cell Biol. 2003 Jan;23(2):733–743. [PMC free article] [PubMed]
  • Lin FL, Sperle K, Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol. 1984 Jun;4(6):1020–1034. [PMC free article] [PubMed]
  • Lin Y, Lukacsovich T, Waldman AS. Multiple pathways for repair of DNA double-strand breaks in mammalian chromosomes. Mol Cell Biol. 1999 Dec;19(12):8353–8360. [PMC free article] [PubMed]
  • Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, Yamaguchi-Iwai Y, Shinohara A, Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998 Sep 15;17(18):5497–5508. [PMC free article] [PubMed]
  • Virgin JB, Bailey JP, Hasteh F, Neville J, Cole A, Tromp G. Crossing over is rarely associated with mitotic intragenic recombination in Schizosaccharomyces pombe. Genetics. 2001 Jan;157(1):63–77. [PMC free article] [PubMed]
  • Malkova A, Ivanov EL, Haber JE. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7131–7136. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...