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PMID: 10353897 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

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

Genetics ·Vol. 152 ·No. 2 ·1999-06-00 ·Pages 529-42

Sekelsky JJ, McKim KS, Messina L, French RL, Hurley WD, Arbel T, Chin GM, Deneen B, Force SJ, Hari KL, Jang JK, Laurençon AC, Madden LD, Matthies HJ, Milliken DB, Page SL, Ring AD, Wayson SM, Zimmerman CC, Hawley RS

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.

MeSH Terms
Animals Chromosomes/genetics DNA/genetics DNA Transposable Elements/genetics Drosophila melanogaster/genetics Female Genes, Insect Heterochromatin Male Meiosis/genetics Metaphase Mutation Nondisjunction, Genetic Phenotype Recombination, Genetic Research Design X Chromosome/genetics
Chemicals
DNA Transposable Elements Heterochromatin DNA
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Sekelsky J J
Department of Genetics, Section of Molecular and Cellular Biology, University of California, Davis, California 95616, USA.
McKim K S
Messina L
French R L
Hurley W D
Arbel T
Chin G M
Deneen B
Force S J
Hari K L
Jang J K
Laurençon A C
Madden L D
Matthies H J
Milliken D B
Page S L
Ring A D
Wayson S M
Zimmerman C C
Hawley R S
References (47)
47 references, click to expand
  1. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories.
    Nat Genet. 1996 Dec;14(4):406-14 PMID: 8944020
  2. Enhancement of the ncdD microtubule motor mutant by mutants of alpha Tub67C.
    J Cell Sci. 1997 Jan;110 ( Pt 2):229-37 PMID: 9044053
  3. Damage control: the pleiotropy of DNA repair genes in Drosophila melanogaster.
    Genetics. 1998 Apr;148(4):1587-98 PMID: 9560378
  4. 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):1867-82 PMID: 9691043
  5. Direct evidence of a role for heterochromatin in meiotic chromosome segregation.
    Cell. 1996 Jul 12;86(1):135-46 PMID: 8689681
  6. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster.
    Genetics. 1972 Jun;71(2):255-86 PMID: 4625747
  7. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family.
    Cell. 1997 Feb 7;88(3):375-84 PMID: 9039264
  8. Mutants affecting meiosis in natural populations of Drosophila melanogaster.
    Genetics. 1968 Nov;60(3):525-58 PMID: 5728740
  9. A functionally specialized alpha-tubulin is required for oocyte meiosis and cleavage mitoses in Drosophila.
    Development. 1993 Mar;117(3):977-91 PMID: 8325246
  10. DNA-replication checkpoint control at the Drosophila midblastula transition.
    Nature. 1997 Jul 3;388(6637):93-7 PMID: 9214509
  11. The Drosophila endocycle is controlled by Cyclin E and lacks a checkpoint ensuring S-phase completion.
    Genes Dev. 1996 Oct 1;10(19):2514-26 PMID: 8843202
  12. Anastral meiotic spindle morphogenesis: role of the non-claret disjunctional kinesin-like protein.
    J Cell Biol. 1996 Jul;134(2):455-64 PMID: 8707829
  13. 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 PMID: 8244010
  14. 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):887-96 PMID: 9490633
  15. Meiotic synapsis in the absence of recombination.
    Science. 1998 Feb 6;279(5352):876-8 PMID: 9452390
  16. P transposon-induced dominant enhancer mutations of position-effect variegation in Drosophila melanogaster.
    Genetics. 1993 Feb;133(2):279-90 PMID: 8382174
  17. Identification of ORD, a Drosophila protein essential for sister chromatid cohesion.
    EMBO J. 1996 Mar 15;15(6):1451-9 PMID: 8635478
  18. Cdks and the Drosophila cell cycle.
    Curr Opin Genet Dev. 1997 Feb;7(1):17-22 PMID: 9024630
  19. A P1-based physical map of the Drosophila euchromatic genome.
    Genome Res. 1996 May;6(5):414-30 PMID: 8743991
  20. The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation.
    Genetics. 1992 Apr;130(4):827-41 PMID: 1582560
  21. Separation of meiotic and mitotic effects of claret non-disjunctional on chromosome segregation in Drosophila.
    EMBO J. 1991 Feb;10(2):419-24 PMID: 1825056
  22. 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):825-35 PMID: 8349113
  23. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector.
    Genes Dev. 1989 Sep;3(9):1273-87 PMID: 2558049
  24. The Trithorax-like gene encodes the Drosophila GAGA factor.
    Nature. 1994 Oct 27;371(6500):806-8 PMID: 7935842
  25. 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):815-21 PMID: 7671309
  26. Mutations in the Drosophila pushover gene confer increased neuronal excitability and spontaneous synaptic vesicle fusion.
    Genetics. 1996 Apr;142(4):1215-23 PMID: 8846899
  27. Requiem for distributive segregation: achiasmate segregation in Drosophila females.
    Trends Genet. 1993 Sep;9(9):310-7 PMID: 8236460
  28. Meiotic segregation in Drosophila melanogaster females: molecules, mechanisms, and myths.
    Annu Rev Genet. 1993;27:281-317 PMID: 8122905
  29. Insertional mutagenesis of the Drosophila genome with single P elements.
    Science. 1988 Mar 4;239(4844):1121-8 PMID: 2830671
  30. 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):2711-23 PMID: 9732269
  31. A stable genomic source of P element transposase in Drosophila melanogaster.
    Genetics. 1988 Mar;118(3):461-70 PMID: 2835286
  32. The Utilization during Mitotic Cell Division of Loci Controlling Meiotic Recombination and Disjunction in DROSOPHILA MELANOGASTER.
    Genetics. 1978 Nov;90(3):531-78 PMID: 17248870
  33. Chromosome segregation influenced by two alleles of the meiotic mutant c(3)G in Drosophila melanogaster.
    Genetics. 1972 Jul;71(3):367-400 PMID: 4624918
  34. Meiosis as an "M" thing: twenty-five years of meiotic mutants in Drosophila.
    Genetics. 1993 Nov;135(3):613-8 PMID: 8293967
  35. Mediation of meiotic and early mitotic chromosome segregation in Drosophila by a protein related to kinesin.
    Nature. 1990 May 3;345(6270):81-3 PMID: 1691829
  36. Recovery and characterization of hybrid dysgenesis-induced mei-9 and mei-41 alleles of Drosophila melanogaster.
    Mutat Res. 1990 Mar;229(1):17-28 PMID: 2156158
  37. On recombination-defective meiotic mutants in Drosophila melanogaster.
    Genetics. 1974 Mar;76(3):453-75 PMID: 4208856
  38. The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1.
    Genetics. 1995 Oct;141(2):619-27 PMID: 8647398
  39. There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology.
    Dev Genet. 1992;13(6):440-67 PMID: 1304424
  40. 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):801-21 PMID: 2503421
  41. Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II.
    Nat Genet. 1996 Dec;14(4):400-5 PMID: 8944019
  42. 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):10824-30 PMID: 7479892
  43. MUTATION, CHROMOSOME NON-DISJUNCTION AND THE GENE.
    Science. 1928 Aug 31;68(1757):211-2 PMID: 17788403
  44. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis.
    Science. 1996 Jul 5;273(5271):118-22 PMID: 8658180
  45. Cloning of the Drosophila melanogaster meiotic recombination gene mei-218: a genetic and molecular analysis of interval 15E.
    Genetics. 1996 Sep;144(1):215-28 PMID: 8878687
  46. Non-Disjunction as Proof of the Chromosome Theory of Heredity (Concluded).
    Genetics. 1916 Mar;1(2):107-63 PMID: 17245853
  47. 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):2932-42 PMID: 9744869
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1999-06-00
Pages
529-42
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1460643
Subset
IM
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