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. 1999 Jun;152(2):529–542. doi: 10.1093/genetics/152.2.529

Identification of novel Drosophila meiotic genes recovered in a P-element screen.

J J Sekelsky 1, K S McKim 1, L Messina 1, R L French 1, W D Hurley 1, T Arbel 1, G M Chin 1, B Deneen 1, S J Force 1, K L Hari 1, J K Jang 1, A C Laurençon 1, L D Madden 1, H J Matthies 1, D B Milliken 1, S L Page 1, A D Ring 1, S M Wayson 1, C C Zimmerman 1, R S Hawley 1
PMCID: PMC1460643  PMID: 10353897

Abstract

The segregation of homologous chromosomes from one another is the essence of meiosis. In many organisms, accurate segregation is ensured by the formation of chiasmata resulting from crossing over. Drosophila melanogaster females use this type of recombination-based system, but they also have mechanisms for segregating achiasmate chromosomes with high fidelity. We describe a P-element mutagenesis and screen in a sensitized genetic background to detect mutations that impair meiotic chromosome pairing, recombination, or segregation. Our screen identified two new recombination-deficient mutations: mei-P22, which fully eliminates meiotic recombination, and mei-P26, which decreases meiotic exchange by 70% in a polar fashion. We also recovered an unusual allele of the ncd gene, whose wild-type product is required for proper structure and function of the meiotic spindle. However, the screen yielded primarily mutants specifically defective in the segregation of achiasmate chromosomes. Although most of these are alleles of previously undescribed genes, five were in the known genes alphaTubulin67C, CycE, push, and Trl. The five mutations in known genes produce novel phenotypes for those genes.

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Selected References

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  1. Baker B. S., Carpenter A. T. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics. 1972 Jun;71(2):255–286. doi: 10.1093/genetics/71.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker B. S., Carpenter A. T., Ripoll P. The Utilization during Mitotic Cell Division of Loci Controlling Meiotic Recombination and Disjunction in DROSOPHILA MELANOGASTER. Genetics. 1978 Nov;90(3):531–578. doi: 10.1093/genetics/90.3.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bickel S. E., Wyman D. W., Miyazaki W. Y., Moore D. P., Orr-Weaver T. L. Identification of ORD, a Drosophila protein essential for sister chromatid cohesion. EMBO J. 1996 Mar 15;15(6):1451–1459. [PMC free article] [PubMed] [Google Scholar]
  4. Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
  5. Bridges C. B. Non-Disjunction as Proof of the Chromosome Theory of Heredity (Concluded). Genetics. 1916 Mar;1(2):107–163. doi: 10.1093/genetics/1.2.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carpenter A. T., Sandler L. On recombination-defective meiotic mutants in Drosophila melanogaster. Genetics. 1974 Mar;76(3):453–475. doi: 10.1093/genetics/76.3.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Cooley L., Kelley R., Spradling A. Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988 Mar 4;239(4844):1121–1128. doi: 10.1126/science.2830671. [DOI] [PubMed] [Google Scholar]
  9. Dernburg A. F., Sedat J. W., Hawley R. S. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996 Jul 12;86(1):135–146. doi: 10.1016/s0092-8674(00)80084-7. [DOI] [PubMed] [Google Scholar]
  10. Dorn R., Szidonya J., Korge G., Sehnert M., Taubert H., Archoukieh E., Tschiersch B., Morawietz H., Wustmann G., Hoffmann G. P transposon-induced dominant enhancer mutations of position-effect variegation in Drosophila melanogaster. Genetics. 1993 Feb;133(2):279–290. doi: 10.1093/genetics/133.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Farkas G., Gausz J., Galloni M., Reuter G., Gyurkovics H., Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. doi: 10.1038/371806a0. [DOI] [PubMed] [Google Scholar]
  13. Follette P. J., O'Farrell P. H. Cdks and the Drosophila cell cycle. Curr Opin Genet Dev. 1997 Feb;7(1):17–22. doi: 10.1016/s0959-437x(97)80104-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ghabrial A., Ray R. P., Schüpbach T. okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev. 1998 Sep 1;12(17):2711–2723. doi: 10.1101/gad.12.17.2711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gowen J. W. MUTATION, CHROMOSOME NON-DISJUNCTION AND THE GENE. Science. 1928 Aug 31;68(1757):211–212. doi: 10.1126/science.68.1757.211. [DOI] [PubMed] [Google Scholar]
  16. Hall J. C. Chromosome segregation influenced by two alleles of the meiotic mutant c(3)G in Drosophila melanogaster. Genetics. 1972 Jul;71(3):367–400. doi: 10.1093/genetics/71.3.367. [DOI] [PubMed] [Google Scholar]
  17. Hari K. L., Santerre A., Sekelsky J. J., McKim K. S., Boyd J. B., Hawley R. S. The mei-41 gene of D. melanogaster is a structural and functional homolog of the human ataxia telangiectasia gene. Cell. 1995 Sep 8;82(5):815–821. doi: 10.1016/0092-8674(95)90478-6. [DOI] [PubMed] [Google Scholar]
  18. Hawley R. S., Irick H., Zitron A. E., Haddox D. A., Lohe A., New C., Whitley M. D., Arbel T., Jang J., McKim K. There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev Genet. 1992;13(6):440–467. doi: 10.1002/dvg.1020130608. [DOI] [PubMed] [Google Scholar]
  19. Hawley R. S., McKim K. S., Arbel T. Meiotic segregation in Drosophila melanogaster females: molecules, mechanisms, and myths. Annu Rev Genet. 1993;27:281–317. doi: 10.1146/annurev.ge.27.120193.001433. [DOI] [PubMed] [Google Scholar]
  20. Hawley R. S. Meiosis as an "M" thing: twenty-five years of meiotic mutants in Drosophila. Genetics. 1993 Nov;135(3):613–618. doi: 10.1093/genetics/135.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Karpen G. H., Le M. H., Le H. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science. 1996 Jul 5;273(5271):118–122. doi: 10.1126/science.273.5271.118. [DOI] [PubMed] [Google Scholar]
  23. Keeney S., Giroux C. N., Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997 Feb 7;88(3):375–384. doi: 10.1016/s0092-8674(00)81876-0. [DOI] [PubMed] [Google Scholar]
  24. Kerrebrock A. W., Miyazaki W. Y., Birnby D., Orr-Weaver T. L. The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics. 1992 Apr;130(4):827–841. doi: 10.1093/genetics/130.4.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kimmerly W., Stultz K., Lewis S., Lewis K., Lustre V., Romero R., Benke J., Sun D., Shirley G., Martin C. A P1-based physical map of the Drosophila euchromatic genome. Genome Res. 1996 May;6(5):414–430. doi: 10.1101/gr.6.5.414. [DOI] [PubMed] [Google Scholar]
  26. Koehler K. E., Boulton C. L., Collins H. E., French R. L., Herman K. C., Lacefield S. M., Madden L. D., Schuetz C. D., Hawley R. S. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nat Genet. 1996 Dec;14(4):406–414. doi: 10.1038/ng1296-406. [DOI] [PubMed] [Google Scholar]
  27. Komma D. J., Endow S. A. Enhancement of the ncdD microtubule motor mutant by mutants of alpha Tub67C. J Cell Sci. 1997 Jan;110(Pt 2):229–237. doi: 10.1242/jcs.110.2.229. [DOI] [PubMed] [Google Scholar]
  28. Komma D. J., Horne A. S., Endow S. A. Separation of meiotic and mitotic effects of claret non-disjunctional on chromosome segregation in Drosophila. EMBO J. 1991 Feb;10(2):419–424. doi: 10.1002/j.1460-2075.1991.tb07963.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Lamb N. E., Freeman S. B., Savage-Austin A., Pettay D., Taft L., Hersey J., Gu Y., Shen J., Saker D., May K. M. Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II. Nat Genet. 1996 Dec;14(4):400–405. doi: 10.1038/ng1296-400. [DOI] [PubMed] [Google Scholar]
  30. Lilly M. A., Spradling A. C. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion. Genes Dev. 1996 Oct 1;10(19):2514–2526. doi: 10.1101/gad.10.19.2514. [DOI] [PubMed] [Google Scholar]
  31. Mathe E., Boros I., Josvay K., Li K., Puro J., Kaufman T. C., Szabad J. The Tomaj mutant alleles of alpha Tubulin67C reveal a requirement for the encoded maternal specific tubulin isoform in the sperm aster, the cleavage spindle apparatus and neurogenesis during embryonic development in Drosophila. J Cell Sci. 1998 Apr;111(Pt 7):887–896. doi: 10.1242/jcs.111.7.887. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Matthies H. J., McDonald H. B., Goldstein L. S., Theurkauf W. E. Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein. J Cell Biol. 1996 Jul;134(2):455–464. doi: 10.1083/jcb.134.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McKim K. S., Dahmus J. B., Hawley R. S. Cloning of the Drosophila melanogaster meiotic recombination gene mei-218: a genetic and molecular analysis of interval 15E. Genetics. 1996 Sep;144(1):215–228. doi: 10.1093/genetics/144.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McKim K. S., Green-Marroquin B. L., Sekelsky J. J., Chin G., Steinberg C., Khodosh R., Hawley R. S. Meiotic synapsis in the absence of recombination. Science. 1998 Feb 6;279(5352):876–878. doi: 10.1126/science.279.5352.876. [DOI] [PubMed] [Google Scholar]
  36. McKim K. S., Hayashi-Hagihara A. mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 1998 Sep 15;12(18):2932–2942. doi: 10.1101/gad.12.18.2932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Richards S., Hillman T., Stern M. Mutations in the Drosophila pushover gene confer increased neuronal excitability and spontaneous synaptic vesicle fusion. Genetics. 1996 Apr;142(4):1215–1223. doi: 10.1093/genetics/142.4.1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sandler L., Lindsley D. L., Nicoletti B., Trippa G. Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics. 1968 Nov;60(3):525–558. doi: 10.1093/genetics/60.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Secombe J., Pispa J., Saint R., Richardson H. Analysis of a Drosophila cyclin E hypomorphic mutation suggests a novel role for cyclin E in cell proliferation control during eye imaginal disc development. Genetics. 1998 Aug;149(4):1867–1882. doi: 10.1093/genetics/149.4.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sekelsky J. J., Burtis K. C., Hawley R. S. Damage control: the pleiotropy of DNA repair genes in Drosophila melanogaster. Genetics. 1998 Apr;148(4):1587–1598. doi: 10.1093/genetics/148.4.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sekelsky J. J., McKim K. S., Chin G. M., Hawley R. S. The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics. 1995 Oct;141(2):619–627. doi: 10.1093/genetics/141.2.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sibon O. C., Stevenson V. A., Theurkauf W. E. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature. 1997 Jul 3;388(6637):93–97. doi: 10.1038/40439. [DOI] [PubMed] [Google Scholar]
  44. Spradling A. C., Stern D. M., Kiss I., Roote J., Laverty T., Rubin G. M. Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):10824–10830. doi: 10.1073/pnas.92.24.10824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Whyte W. L., Irick H., Arbel T., Yasuda G., French R. L., Falk D. R., Hawley R. S. The genetic analysis of achiasmate segregation in Drosophila melanogaster. III. The wild-type product of the Axs gene is required for the meiotic segregation of achiasmate homologs. Genetics. 1993 Jul;134(3):825–835. doi: 10.1093/genetics/134.3.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yamamoto A. H., Brodberg R. K., Banga S. S., Boyd J. B., Mason J. M. Recovery and characterization of hybrid dysgenesis-induced mei-9 and mei-41 alleles of Drosophila melanogaster. Mutat Res. 1990 Mar;229(1):17–28. doi: 10.1016/0027-5107(90)90004-n. [DOI] [PubMed] [Google Scholar]
  47. Zitron A. E., Hawley R. S. The genetic analysis of distributive segregation in Drosophila melanogaster. I. Isolation and characterization of Aberrant X segregation (Axs), a mutation defective in chromosome partner choice. Genetics. 1989 Aug;122(4):801–821. doi: 10.1093/genetics/122.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]

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