Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1995 Apr;139(4):1585–1599. doi: 10.1093/genetics/139.4.1585

Horka, a Dominant Mutation of Drosophila, Induces Nondisjunction And, through Paternal Effect, Chromosome Loss and Genetic Mosaics

J Szabad 1, E Mathe 1, J Puro 1
PMCID: PMC1206486  PMID: 7789762

Abstract

Fs(3) Horka (Horka) was described as a dominant female-sterile mutation of Drosophila melanogaster. Genetic and cytological data show that Horka induces mostly equational nondisjunction during spermatogenesis but not chromosome loss and possesses a dominant paternal effect: the X, second, third and the fourth chromosomes, but not the Y, are rendered unstable while undergoing spermatogenesis and may be lost in the descending zygotes. The frequency of Horka-induced chromosome loss is usually 2-4% but varies with the genetic background and can be over 20%. The X chromosome loss occurs during the gonomeric and the initial cleavage divisions. Loss of the X and fourth chromosomes shows no correlation. We propose, based on similarities in the mutant phenotypes with the chromosome destabilizing mutations nonclaret disjunctional and paternal loss, that the normal Horka(+) product is required for function of the centromeres and/or nearby regions. Horka is a convenient tool for the generation of gynandromorphs, autosome mosaics and for the study of gene expression in mosaics.

Full Text

The Full Text of this article is available as a PDF (4.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baker B. S. Paternal loss (pal): a meiotic mutant in Drosophila melanogaster causing loss of paternal chromosomes. Genetics. 1975 Jun;80(2):267–296. doi: 10.1093/genetics/80.2.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bellen H. J., O'Kane C. J., Wilson C., Grossniklaus U., Pearson R. K., Gehring W. J. P-element-mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 1989 Sep;3(9):1288–1300. doi: 10.1101/gad.3.9.1288. [DOI] [PubMed] [Google Scholar]
  3. Bopp D., Bell L. R., Cline T. W., Schedl P. Developmental distribution of female-specific Sex-lethal proteins in Drosophila melanogaster. Genes Dev. 1991 Mar;5(3):403–415. doi: 10.1101/gad.5.3.403. [DOI] [PubMed] [Google Scholar]
  4. Boyd J. B., Golino M. D., Shaw K. E., Osgood C. J., Green M. M. Third-chromosome mutagen-sensitive mutants of Drosophila melanogaster. Genetics. 1981 Mar-Apr;97(3-4):607–623. doi: 10.1093/genetics/97.3-4.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brunner D., Oellers N., Szabad J., Biggs W. H., 3rd, Zipursky S. L., Hafen E. A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell. 1994 Mar 11;76(5):875–888. doi: 10.1016/0092-8674(94)90362-x. [DOI] [PubMed] [Google Scholar]
  6. Castrillon D. H., Gönczy P., Alexander S., Rawson R., Eberhart C. G., Viswanathan S., DiNardo S., Wasserman S. A. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. doi: 10.1093/genetics/135.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis D. G. Chromosome Behavior under the Influence of Claret-Nondisjunctional in DROSOPHILA MELANOGASTER. Genetics. 1969 Mar;61(3):577–594. doi: 10.1093/genetics/61.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Endow S. A. Chromosome distribution, molecular motors and the claret protein. Trends Genet. 1993 Feb;9(2):52–55. doi: 10.1016/0168-9525(93)90187-M. [DOI] [PubMed] [Google Scholar]
  9. Endow S. A., Henikoff S., Soler-Niedziela L. Mediation of meiotic and early mitotic chromosome segregation in Drosophila by a protein related to kinesin. Nature. 1990 May 3;345(6270):81–83. doi: 10.1038/345081a0. [DOI] [PubMed] [Google Scholar]
  10. Endow S. A. Meiotic chromosome distribution in Drosophila oocytes: roles of two kinesin-related proteins. Chromosoma. 1992 Dec;102(1):1–8. doi: 10.1007/BF00352283. [DOI] [PubMed] [Google Scholar]
  11. Erdélyi M., Szabad J. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome. Genetics. 1989 May;122(1):111–127. doi: 10.1093/genetics/122.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Garcia-Bellido A., Merriam J. R. Clonal parameters of tergite development in Drosophila. Dev Biol. 1971 Oct;26(2):264–276. doi: 10.1016/0012-1606(71)90126-6. [DOI] [PubMed] [Google Scholar]
  13. Gausz J., Gyurkovics H., Bencze G., Awad A. A., Holden J. J., Ish-Horowicz D. Genetic characterization of the region between 86F1,2 and 87B15 on chromosome 3 of Drosophila melanogaster. Genetics. 1981 Aug;98(4):775–789. doi: 10.1093/genetics/98.4.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gelbart W. M. A new mutant controlling mitotic chromosome disjunction in Drosophila melanogaster. Genetics. 1974 Jan;76(1):51–63. doi: 10.1093/genetics/76.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Glover D. M. Mitosis in the Drosophila embryo--in and out of control. Trends Genet. 1991 Apr;7(4):125–132. doi: 10.1016/0168-9525(91)90457-2. [DOI] [PubMed] [Google Scholar]
  16. González C., Casal J., Ripoll P. Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. Genet Res. 1989 Dec;54(3):205–212. doi: 10.1017/s0016672300028664. [DOI] [PubMed] [Google Scholar]
  17. Govind S., Steward R. Dorsoventral pattern formation in Drosophila: signal transduction and nuclear targeting. Trends Genet. 1991 Apr;7(4):119–125. doi: 10.1016/0168-9525(91)90456-z. [DOI] [PubMed] [Google Scholar]
  18. Guerra M., Postlethwait J. H., Schneiderman H. A. The development of the imaginal abdomen of Drosophila melanogaster. Dev Biol. 1973 Jun;32(2):361–372. doi: 10.1016/0012-1606(73)90247-9. [DOI] [PubMed] [Google Scholar]
  19. Hawley R. S., Theurkauf W. E. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 1993 Sep;9(9):310–317. doi: 10.1016/0168-9525(93)90249-h. [DOI] [PubMed] [Google Scholar]
  20. Janning W. Gynandromorph fate maps in Drosophila. Results Probl Cell Differ. 1978;9:1–28. doi: 10.1007/978-3-540-35803-9_1. [DOI] [PubMed] [Google Scholar]
  21. Karr T. L. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech Dev. 1991 Jun;34(2-3):101–111. doi: 10.1016/0925-4773(91)90047-a. [DOI] [PubMed] [Google Scholar]
  22. Kastenbaum M. A., Bowman K. O. Tables for determining the statistical significance of mutation frequencies. Mutat Res. 1970 May;9(5):527–549. doi: 10.1016/0027-5107(70)90038-2. [DOI] [PubMed] [Google Scholar]
  23. Klingler M., Erdélyi M., Szabad J., Nüsslein-Volhard C. Function of torso in determining the terminal anlagen of the Drosophila embryo. Nature. 1988 Sep 15;335(6187):275–277. doi: 10.1038/335275a0. [DOI] [PubMed] [Google Scholar]
  24. Lin H. F., Wolfner M. F. The Drosophila maternal-effect gene fs(1)Ya encodes a cell cycle-dependent nuclear envelope component required for embryonic mitosis. Cell. 1991 Jan 11;64(1):49–62. doi: 10.1016/0092-8674(91)90208-g. [DOI] [PubMed] [Google Scholar]
  25. Matthews K. A., Rees D., Kaufman T. C. A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila. Development. 1993 Mar;117(3):977–991. doi: 10.1242/dev.117.3.977. [DOI] [PubMed] [Google Scholar]
  26. McDonald H. B., Goldstein L. S. Identification and characterization of a gene encoding a kinesin-like protein in Drosophila. Cell. 1990 Jun 15;61(6):991–1000. doi: 10.1016/0092-8674(90)90064-l. [DOI] [PubMed] [Google Scholar]
  27. McDonald H. B., Stewart R. J., Goldstein L. S. The kinesin-like ncd protein of Drosophila is a minus end-directed microtubule motor. Cell. 1990 Dec 21;63(6):1159–1165. doi: 10.1016/0092-8674(90)90412-8. [DOI] [PubMed] [Google Scholar]
  28. Merriam J. R., Nöthiger R., Garcia-Bellido A. Are dicentric anaphase bridges formed by somatic recombination in X chromosome inversion heterozygotes of Drosophila melanogaster? Mol Gen Genet. 1972;115(4):294–301. doi: 10.1007/BF00333168. [DOI] [PubMed] [Google Scholar]
  29. Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
  30. Puro J. Differential mechanisms governing segregation of a univalent in oocytes and spermatocytes of Drosophila melanogaster. Chromosoma. 1991 Jun;100(5):305–314. doi: 10.1007/BF00360529. [DOI] [PubMed] [Google Scholar]
  31. Sequeira W., Nelson C. R., Szauter P. Genetic analysis of the claret locus of Drosophila melanogaster. Genetics. 1989 Nov;123(3):511–524. doi: 10.1093/genetics/123.3.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. St Johnston D., Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell. 1992 Jan 24;68(2):201–219. doi: 10.1016/0092-8674(92)90466-p. [DOI] [PubMed] [Google Scholar]
  33. Szabad J., Erdélyi M., Hoffmann G., Szidonya J., Wright T. R. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. II. Mutations on the second chromosome. Genetics. 1989 Aug;122(4):823–835. doi: 10.1093/genetics/122.4.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Szabad J., Nöthiger R. Gynandromorphs of Drosophila suggest one common primordium for the somatic cells of the female and male gonads in the region of abdominal segments 4 and 5. Development. 1992 Jun;115(2):527–533. doi: 10.1242/dev.115.2.527. [DOI] [PubMed] [Google Scholar]
  35. Szabad J., Schüpbach T., Wieschaus E. Cell lineage and development in the larval epidermis of Drosophila melanogaster. Dev Biol. 1979 Dec;73(2):256–271. doi: 10.1016/0012-1606(79)90066-6. [DOI] [PubMed] [Google Scholar]
  36. Sánchez L., Nöthiger R. Sex determination and dosage compensation in Drosophila melanogaster: production of male clones in XX females. EMBO J. 1983;2(4):485–491. doi: 10.1002/j.1460-2075.1983.tb01451.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Theurkauf W. E., Hawley R. S. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol. 1992 Mar;116(5):1167–1180. doi: 10.1083/jcb.116.5.1167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wright T. R. The genetics of embryogenesis in Drosophila. Adv Genet. 1970;15:261–395. doi: 10.1016/s0065-2660(08)60075-9. [DOI] [PubMed] [Google Scholar]
  39. Yamamoto A. H., Komma D. J., Shaffer C. D., Pirrotta V., Endow S. A. The claret locus in Drosophila encodes products required for eyecolor and for meiotic chromosome segregation. EMBO J. 1989 Dec 1;8(12):3543–3552. doi: 10.1002/j.1460-2075.1989.tb08526.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zalokar M., Erk I., Santamaría P. Distribution of ring-X chromosomes in the blastoderm of gynandromorphic D. melanogaster. Cell. 1980 Jan;19(1):133–141. doi: 10.1016/0092-8674(80)90394-3. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES