The mus309 mutation, defective in DNA double-strand break repair, increases the frequency of X-ray-induced somatic crossing over in Drosophila melanogaster, but the effect is not dose-rate dependent


Effect of a 1000 R dose of hard X-rays, with two different dose-rates viz. 300 and 1000 R/min on somatic crossing over in the X chromosome of Drosophila melanogaster was studied in two different genotypes. Irradiation was given during the first-instar larval stage of the development. In the control crosses the flies carried wild-type autosomes, but in the experimental crosses the 3rd chromosomes carried a DNA double-strand break repair deficient mus309 mutant gene constitution. As expected, the frequency of X-ray-induced somatic crossing over increased in the mutant flies with both dose-rates of irradiation. As also expected, in the control flies irradiation given with the 300 R/min dose-rate caused more somatic crossovers than irradiation given with the 1000 R/ min rate. However, rather unexpectedly, in the experimental flies there was no significant difference in the frequency of somatic crossing over between the two dose-rates of irradiation. The results can be explained by assuming that X-ray-induced somatic crossing over is a two-step event, and that the mechanism which repairs the lesion caused by the irradiation is controlled by the mus309 gene. In the control flies the repairing mechanism is capable to recover if the irradiation is given with a short term high dose-rate, but is not capable to recover if the irradiation is given with a long lasting low dose-rate. However, in the experimental mutant flies the repairing mechanism is only poorly recovered irrespective of the dose-rate.

Share and Cite:

Portin, P. (2012) The mus309 mutation, defective in DNA double-strand break repair, increases the frequency of X-ray-induced somatic crossing over in Drosophila melanogaster, but the effect is not dose-rate dependent. Open Journal of Genetics, 2, 39-46. doi: 10.4236/ojgen.2012.21004.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Mahaney, B.L., Meek, K. and Lees-Miller, S.P. (2009) Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous endjoining. Biochemical Journal, 417, 639-650.
[2] Hartlerode, A.J. and Scully, R. (2009) Mechanisms of double-strand break repair in somatic mammalian cells. Biochemical Journal, 423, 157-168. doi:10.1042/BJ20090942
[3] Paques, F. and Haber, J.E. (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews, 63, 349-404.
[4] Sung, P. and Klein, H. (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nature Reviews Molecular Cell Biology, 7, 739-750. doi:10.1038/nrm2008
[5] Helleday, T., Lo, J., van Gent, D.C. and Engelward, B.P. (2007) DNA double-strand break repair: From mechanistic understanding to cancer treatment. DNA Repair, 6, 923-935. doi:10.1016/j.dnarep.2007.02.006
[6] Rothkamm, K., Kruger, I., Thompson, L.H. and Lobrich, M. (2007) Pathways of DNA double-strand break repair during the mammalian cell cycle. Molecular and Cellular Biology, 23, 5706-5715. doi:10.1128/MCB.23.16.5706-5715.2003
[7] Branzei, D. and Foiani, M. (2008) Regulation of DNA repair throughout the cell cycle. Nature Reviews Molecular Cell Biology, 9, 297-308. doi:10.1038/nrm2351
[8] Symington, L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiology and Molecular Biology Reviews, 66, 630-670. doi:10.1128/MMBR.66.4.630-670.2002
[9] Heyer, W-D., Ehmsen, K.T. and Solinger, J.A. (2003) Holliday junctions in eukaryotic nucleus: Resolution in sight? Trends in Biochemical Sciences, 28, 548-557. doi:10.1016/j.tibs.2003.08.011
[10] Heyer, W-D. (2004) Recombination: Holliday junction resolution and crossover formation. Current Biology, 14, R56-R58. doi:10.1016/j.cub.2003.12.043
[11] Boyd, J.B., Golino, M.D., Shaw, K.E.S., Osgood, C.J. and Green, M.M. (1981) Third-chromosome mutagen-sensitive mutants of Drosophila melanogaster. Genetics, 97, 607- 623
[12] Ellis, N.A., Groden, J., Ye, T-Z., Staughen, J., Lennon, D.J., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom’s syndrome gene-product is homologous to RecQ helicases. Cell, 83, 655-666. doi:10.1016/0092-8674(95)90105-1
[13] Karow, J.K., Chakraverty, R.K. and Hickson, J.D. (1997) The Bloom’s syndrome gene product is a 3’- 5’ DNA helicase. Journal of Biological Chemistry, 272, 30611- 30614. doi:10.1074/jbc.272.49.30611
[14] Mohaghegh, P., Karow, J.K., Brosh, R.M. Jr., Bohr, V.A. and Hickson, I.D. (2001) The Bloom’s and Werner’s syndrome proteins are DNA structure-specific homologues. Nucleic Acids Research, 29, 2843-2849. doi:10.1093/nar/29.13.2843
[15] Wu, L., Davies, S.L., Levitt, N.C. and Hickson, I.D. (2001) Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD5. Journal of Biological Chemistry, 276, 19375-19381. doi:10.1074/jbc.M009471200
[16] Van Brabant, A.J., Stan, R. and Ellis, N.A. (2000) DNA helicases, genome instability, and human genetic disease. Annual Reviews of Genomics and Human Genetics, 1, 409-459. doi:10.1146/annurev.genom.1.1.409
[17] Kooistra, R., Pastink, A., Zonneveld, J.B.M., Lohman, P.H.M. and Eeken, J.C.J. (1999)The Drosophila melano- gaster DmRAD54 gene plays a crucial role in double-strand break repair after P-element excision and acts synergistically with Ku70 in the repair of X-ray damage. Molecular and Cellular Biology, 19, 6269-6275
[18] Adams, M.D., McVey, M. and Sekelsky, J.J. (2003) Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science, 299, 265-267. doi:10.1126/science.1077198
[19] Laurencon, A., Orme, C.M., Peters, H.K., Boulton, C.L., Vladar, E.K., Langley, S.A., Bakis, E.P., Harris, D.T., Harris, N.J., Wayson, S.M., Hawley, R.S. and Burtis, K.C. (2004) A large-scale screen for mutagen sensitive loci in Drosophila. Genetics, 167, 217-231. doi:10.1534/genetics.167.1.217
[20] Portin, P. (2005) mus309 mutation, defective in DNA double-strand break repair, affects intergenic but not intragenic meiotic recombination in Drosophila melanogaster. Genetical Research, 86, 185-191. doi:10.1017/S0016672305007883
[21] Rockmill, B., Fung, J.C., Branda, S.S. and Roeder, G.S. (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Current Biology, 13, 1954- 1962. doi:10.1016/j.cub.2003.10.059
[22] Johnson-Schlitz, D. and Engels, W.R. (2003) Template disruption and failure of double Holliday junction dissolution during double-strand break repair in Drosophila BLM mutants. Proceedings of the National Academy of Sciences USA, 103, 16840-16845. doi:10.1073/pnas.0607904103
[23] McVey, M., Larocque, J.R., Adams, M.D. and Sekelsky, J.J. (2004) Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proceedings of the National Academy of Sciences USA, 101, 15694-15699. doi:10.1073/pnas.0406157101
[24] McVey, M. andersen, S.L., Broze, J. and Sekelsky, J. (2007) Multiple functions of Drosophila BLM helicase in maintenance of genome stability. Genetics, 176, 1979-1992. doi:10.1534/genetics.106.070052
[25] Trowbridge, K., McKim, K., Brill, S.J. and Sekelsky, J. (2007) Synthetic lethality of Drosophila in the absence of the MUS81 endonuclease and the DmBlm helicase is associated with elevated apoptosis. Genetics, 176, 1993-2001. doi:10.1534/genetics.106.070060
[26] Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J. and Stahl, F.W. (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35. doi:10.1016/0092-8674(83)90331-8
[27] Ira, G., Malkova, A., Liberi, G., Foiani, M. and Haber, J.E. (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell, 115, 401-411. doi:10.1016/S0092-8674(03)00886-9
[28] Wu, L. and Hickson, I.D. (2003) The Bloom’s syndrome helicase suppresses crossing over during homologous recombination. Nature, 426, 870-874. doi:10.1038/nature02253
[29] Stern, C. (1936) Somatic crossing over and segregation in Drosophila melanogaster. Genetics, 21, 625-730.
[30] Patterson, J.T. (1929) The production of mutations in somatic cells of Drosophila melanogaster by means of X-rays. Journal of Experimental Zoology, 53, 327-372. doi:10.1002/jez.1400530302
[31] Ashburner, M. (1989) Drosophila. A Laboratory Hand- book. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
[32] Becker, H.J. (1976) Mitotic recombination. In: Ashburner, M. and Novitki, E., Eds., The Genetics and Biology of Drosophila Vol. 1 c, Academic Press, London, 1019-1087.
[33] Garcia-Bellido, A. (1972) Some parameters of mitotic re- combination in Drosophila melanogaster. Molecular and General Genetics, 115, 54-72. doi:10.1007/BF00272218
[34] Ayaki, T., Fujikawa, K., Ryo, H., Itoh, T. and Kondo, S. (1990) Induced rates of mitotic crossing over and possible mitotic gene conversion per wing anlage cell in Drosophila melanogaster by X rays and fission neutrons. Genetics, 126, 157-166.
[35] Kusano, K., Johnson-Schlitz, D.M. and Engels, W.R. (2001) Sterility of Drosophila with mutations in the Bloom syndrome gene—Complementation by Ku70. Science, 291, 2600-2602. doi:10.1126/science.291.5513.2600
[36] Beal, E.L. and D.C. Rio, D.C. (1996) Drosophila IRBP / Ku p70 corresponds to the mutagen-sensitive mus309 gene and is involved in P-element excision in vivo. Genes and Development, 10, 921-933. doi:10.1101/gad.10.8.921
[37] Allison, P.S. (1999) Logistic regression using the SAS? system: Theory and applications. SAS Institute Inc., Cary.
[38] Kaplan, W.D. (1953) The influence of Minutes upon somatic crossing-over Drosophila melanogaster. Genetics, 38, 630-651.
[39] Walen, K.H. (1964) Somatic crossing over in relationship to heterochromatin in Drosophila melanogaster. Genetics, 49, 905-923.
[40] Ronen, M. (1964) Interchromosomal effects on somatic recombination in Drosophila melanogaster. Genetics, 50, 649-658.
[41] Haendle, J. (1971) R?ntgeninduzierte mitotische Rekom-bination bei Drosophila melanogaster. I. Ihre Abh?ngigkeit von der Dosis, der Dosisrate und vom Spektrum. Molecular and General Genetics, 113, 114-131.
[42] Haendle, J. (1971) R?ntgeninduzierte mitotische Rekombination bei Drosophila melanogaster. II. Beweis der Existenz und Charakterisierung zweier von der Art des Spektrums abh?ngiger Reaktionen. Molecular and General Genetics, 113, 132-149.
[43] Haendle, J. (1974) X-ray induced mitotic recombination in Drosophila melanogaster. III. Dose dependence of the “pairing” component. Molecular and General Genetics, 128, 233-239. doi:10.1007/BF00267112
[44] Haendle, J. (1979) X-ray induced mitotic recombination in Drosophila melanogaster. IV. Distribution within euand heterochromatin. Mutation Research, 62, 467-475. doi:10.1016/0027-5107(79)90042-3
[45] Lindsley, D.L. and Tokuyasu, K.T. (1980) Spermatogenesis. In: Ashburner, M. and Wright, T.R.F., Eds., The Genetics and Biology of Drosophila Vol. 2 d, Academic Press, London, 225-294.
[46] Madhavan, M.M. and Schneiderman, H.A. (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Wilhelm Roux’s Archives of Developmental Biology, 183, 269-305. doi:10.1007/BF00848459

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.