Further evidence for the theory that crossover interference in Drosophila melanogaster is dependent on genetic rather than physical distance between adjacent crossover points

Petter Portin

Laboratory of Genetics, Department of Biology, University of Turku, Turku, Finland.

DOI: 10.4236/ojgen.2012.23020                

Abstract

Effect of heat shock on certain meiotic parameters in Drosophila melanogaster was studied in the cv-v-f region of the X chromosome of females homozygous for mus309 mutation, deficient in DNA double-strand break repair, or being of wild type. The heat shock in the wild females caused that the frequencies of the single crossovers and all the map lengths decreased while the frequency of the double crossovers and crossover interference remained unchanged. In the mus309 mutants all parameters remained unchanged except that single crossovers in the cv-v interval were less frequent, and that crossover interference diminished. Thus, heat shock seems have two separate effects; one being independent on the mus309 gene and affecting the occurrence of crossing over itself, and the other being dependent on the mus309 gene and affecting some precondition of crossing over. This precondition is probably the choice between two routes of the repair of double-strand DNA breaks known to be controlled by the mus309 gene. The results are in accordance with the genetic models of interference in which interference depends on genetic distance between the crossover points, but in contradiction with physical models where interference is dependent on physical distance between the crossover points.

Keywords

Chiasma; Chromosome; Map Length; Meiosis

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Sturtevant, A.H. (1915) The behavior of the chromosomes as studied through linkage. Zeitschrift für Inductive Abstammungs und Vererbungslehre, 13, 234-287.
[2]	Muller, H.J. (1916) The mechanism of crossing over. American Naturalist, 50, 193-221. doi:10.1086/279534
[3]	Hillers, K.J. (2004) Crossover interference. Current Biology, 14, R1036-R1037. doi:10.1016/j.cub.2004.11.038
[4]	Foss, E., Lande, R., Stahl, F.W. and Steinberg, C.M. (1993) Chiasma interference as a function of genetic Edistance. Genetics, 133, 681-691.
[5]	Mortimer, R.K. and Fogel, S. (1974) Genetical interference and gene conversion. In: Grell, R.F., Ed., Mechanims in Recombination, Plenum Press, New York, 263-275. doi:10.1007/978-1-4684-2133-0_23
[6]	Portin, P. (2011) Effect of temperature on crossing over in the mus309 mutant, deficient in DNA double-strand break repair, of Drosophila melanogaster suggests a mechanism for crossover interference. Open Journal of Genetics, 1, 38-47. doi:10.4236/ojgen.2011.13008
[7]	McKim, K.S. and Hayashi-Hagihara, A. (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: Evidence that the mechanism for initiating meiotic recombination is conserved. Genes and Development, 12, 2932-2942. doi:10.1101/gad.12.18.2932
[8]	Olsen-Krogh, B. and Symington, L.S. (2004) Recombination proteins in yeast. Annual Reviews of Genetics, 38, 233-271. doi:10.1146/annurev.genet.38.072902.091500
[9]	Lorenz, A. and Whitby, M.C. (2006) Crossover promotion and prevention. Biochemical Society Transactions, 34, 537-541. doi:10.1042/BST0340537
[10]	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
[11]	Heyer, W.-D. (2004) Recombination: Holliday junction resolution and crossover formation. Current Biology, 14, R56-R58. doi:10.1016/j.cub.2003.12.043
[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 Jr., R.M., 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 RAD51. Journal of Biological Chemistry, 276, 19375-19381. doi:10.1074/jbc.M009471200
[16]	Brabant, A.J. van 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]	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
[18]	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
[19]	Portin, P. (2005) mus309 mutation, defective in DNA double-strand break repair, affects intergenic but not in-tragenic meiotic recombination in Drosophila melano-gaster. Genetical Research, 86, 185-191. doi:10.1017/S0016672305007883
[20]	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
[21]	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
[22]	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.
[23]	Beal, E.L. and 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
[24]	Weinstein, A. (1936) The theory of multiple-strand crossing over. Genetics, 21, 155-199.
[25]	Stevens, W.L. (1936) The analysis of interference. Journal of Genetics, 32, 51-64. doi:10.1007/BF02982501
[26]	Grell, R.F. and Chandley, A.C. (1965) Evidence bearing on the coincidence of exchange and DNA replication in the oocyte of Drosophila melanogaster. Proceedings of the National Academy of Sciences USA, 53, 1340-1346. doi:10.1073/pnas.53.6.1340
[27]	Grell, R.F. (1972) Recombination and DNA replication in the Drosophila melanogaster oocyte. Genetics, 73, 87-108.
[28]	Portin, P. and Suormala, T. (1973) Timing of meiotic crossing-over in Drosophila melanogaster. Hereditas, 75, 267-272. doi:10.1111/j.1601-5223.1973.tb01168.x
[29]	Mehrotra, S. and McKim, K.S. (2006) Temporal analysis of meiotic DNA double-strand break formation and repair in Drosophila females. Public Library of Sciences Genetics, 2, 1883-1897.
[30]	Joyce, E.F. and McKim, K.S. (2009) Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics, 181, 39-51. doi:10.1534/genetics.108.093112
[31]	Baker, B.S. and Hall, J.C. (1976) Meiotic mutants: Genetic control of meiotic recombination and chromosome segregation. In: Ashburner, M. and Novitski, E. Eds., The Genetics and Biology of Drosophila, Vol. 1a, Academic Press, London, 351-434.
[32]	Sandler, L., Lindsley, D.L., Nicoletti, B. and Trippa, G. (1968) Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics, 60, 525-558.
[33]	Baker, B.S. and Carpenter, A.T.C. (1972) Genetic analysis of sex chromosomal meiotic mutants in Drosophila melanogaster. Genetics, 71, 255-286.
[34]	Fujitani, Y., Mori, S. and Kobayashi, I. (2002) A reaction-diffusion model for interference in meiotic crossing over. Genetics, 161, 365-372.