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PMID: 9744869 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S.

mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved.

Genes & development ·Vol. 12 ·No. 18 ·1998-09-15 ·Pages 2932-42

McKim KS, Hayashi-Hagihara A

Abstract

Meiotic recombination requires the action of several gene products in both Saccharomyces cerevisiae and Drosophila melanogaster. Genetic studies in D. melanogaster have shown that the mei-W68 gene is required for all meiotic gene conversion and crossing-over. We cloned mei-W68 using a new genetic mapping method in which P elements are used to promote crossing-over at their insertion sites. This resulted in the high-resolution mapping of mei-W68 to a <18-kb region that contains a homolog of the S. cerevisiae spo11 gene. Molecular analysis of several mutants confirmed that mei-W68 encodes an spo11 homolog. Spo11 and MEI-W68 are members of a family of proteins similar to a novel type II topoisomerase. On the basis of this and other lines of evidence, Spo11 has been proposed to be the enzymatic activity that creates the double-strand breaks needed to initiate meiotic recombination. This raises the possibility that recombination in Drosophila is also initiated by double-strand breaks. Although these homologous genes are required absolutely for recombination in both species, their roles differ in other respects. In contrast to spo11, mei-W68 is not required for synaptonemal complex formation and does have a mitotic role.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Chromosome Mapping Cloning, Molecular Crosses, Genetic Crossing Over, Genetic DNA Primers/genetics DNA Topoisomerases, Type I/genetics DNA, Complementary/genetics Drosophila melanogaster/genetics Female Genes, Insect Insect Proteins/genetics Male Meiosis/genetics Molecular Sequence Data Mutation Polymerase Chain Reaction Recombination, Genetic Saccharomyces cerevisiae/genetics Species Specificity Synaptonemal Complex/genetics
Chemicals
DNA Primers DNA, Complementary Insect Proteins DNA Topoisomerases, Type I
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
McKim K S
Waksman Institute, Rutgers University, Piscataway, New Jersey 08854-8020, USA. mckim@rci.rutgers.edu,
Hayashi-Hagihara A
References (57)
57 references, click to expand
  1. Preferential transposition of Drosophila P elements to nearby chromosomal sites.
    Genetics. 1993 Feb;133(2):347-59 PMID: 8382177
  2. Covalent protein-DNA complexes at the 5' strand termini of meiosis-specific double-strand breaks in yeast.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11274-8 PMID: 7479978
  3. Meiotic recombination hotspots.
    Annu Rev Genet. 1995;29:423-44 PMID: 8825482
  4. Transient, meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe.
    Genetics. 1994 Mar;136(3):769-79 PMID: 8005432
  5. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination.
    Genetics. 1992 Nov;132(3):651-64 PMID: 1468624
  6. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae.
    EMBO J. 1995 Sep 15;14(18):4589-98 PMID: 7556102
  7. Sex and the single cell: meiosis in yeast.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10450-6 PMID: 7479818
  8. Meiosis-induced double-strand break sites determined by yeast chromatin structure.
    Science. 1994 Jan 28;263(5146):515-8 PMID: 8290959
  9. Meiotic roles of crossing-over and of gene conversion.
    Cold Spring Harb Symp Quant Biol. 1984;49:23-9 PMID: 6597757
  10. Spontaneous recombination in Drosophila melanogaster males.
    Proc Natl Acad Sci U S A. 1971 Feb;68(2):268-70 PMID: 5277066
  11. The initiation of meiotic chromosome pairing: the cytological view.
    Genome. 1990 Dec;33(6):759-78 PMID: 2086352
  12. Genetic and molecular analysis of smooth, a quantitative trait locus affecting bristle number in Drosophila melanogaster.
    Genetics. 1997 Jun;146(2):607-18 PMID: 9178010
  13. Genome structure and evolution in Drosophila: applications of the framework P1 map.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6824-9 PMID: 8041703
  14. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster.
    Genetics. 1972 Jun;71(2):255-86 PMID: 4625747
  15. 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
  16. Structure and mechanism of DNA topoisomerase II.
    Nature. 1996 Jan 18;379(6562):225-32 PMID: 8538787
  17. Identification of double Holliday junctions as intermediates in meiotic recombination.
    Cell. 1995 Dec 1;83(5):783-91 PMID: 8521495
  18. Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites.
    Genetics. 1980 Mar;94(3):625-46 PMID: 6772522
  19. An atypical topoisomerase II from Archaea with implications for meiotic recombination.
    Nature. 1997 Mar 27;386(6623):414-7 PMID: 9121560
  20. Purification of a DNA topoisomerase II from the hyperthermophilic archaeon Sulfolobus shibatae. A thermostable enzyme with both bacterial and eucaryal features.
    J Biol Chem. 1994 Nov 4;269(44):27663-9 PMID: 7961685
  21. Mapping of Drosophila mutations using site-specific male recombination.
    Genetics. 1998 May;149(1):157-63 PMID: 9584093
  22. Meiotic synapsis in the absence of recombination.
    Science. 1998 Feb 6;279(5352):876-8 PMID: 9452390
  23. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae.
    Cell. 1990 Jun 15;61(6):1089-101 PMID: 2190690
  24. Flanking duplications and deletions associated with P-induced male recombination in Drosophila.
    Genetics. 1996 Dec;144(4):1623-38 PMID: 8978050
  25. Meiotic chromosomes: it takes two to tango.
    Genes Dev. 1997 Oct 15;11(20):2600-21 PMID: 9334324
  26. Gene conversion, recombination nodules, and the initiation of meiotic synapsis.
    Bioessays. 1987 May;6(5):232-6 PMID: 3606589
  27. Enhancement of spontaneous mitotic recombination by the meiotic mutant spo11-1 in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 1983 Dec;80(24):7566-70 PMID: 6369322
  28. The genetics of meiosis in Caenorhabditis elegans.
    Trends Genet. 1995 Jan;11(1):27-31 PMID: 7900192
  29. A P1-based physical map of the Drosophila euchromatic genome.
    Genome Res. 1996 May;6(5):414-30 PMID: 8743991
  30. A general model for genetic recombination.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):358-61 PMID: 1054510
  31. Selection for male recombination in Drosophila melanogaster.
    Genetics. 1976 Oct;84(2):333-51 PMID: 826449
  32. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  33. The effects of recombination-defective meiotic mutants in Drosophila melanogaster on gonial recombination in males.
    Mutat Res. 1979 Jul;61(2):221-7 PMID: 113674
  34. The role of the SPO11 gene in meiotic recombination in yeast.
    Genetics. 1985 Jun;110(2):187-216 PMID: 3891509
  35. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  36. The RAD50 gene, a member of the double strand break repair epistasis group, is not required for spontaneous mitotic recombination in yeast.
    Curr Genet. 1990 Aug;18(2):111-6 PMID: 2225142
  37. Meiosis: how could it work?
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167-74 PMID: 8710842
  38. Developmental regulation of Drosophila DNA topoisomerase II.
    J Cell Biol. 1991 Jan;112(2):203-13 PMID: 1846370
  39. Isolation, DNA sequence, and regulation of a meiosis-specific eukaryotic recombination gene.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):8035-9 PMID: 3317399
  40. 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
  41. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  42. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate.
    EMBO J. 1995 Sep 15;14(18):4599-608 PMID: 7556103
  43. Mei-S332, a Drosophila protein required for sister-chromatid cohesion, can localize to meiotic centromere regions.
    Cell. 1995 Oct 20;83(2):247-56 PMID: 7585942
  44. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast.
    Cell. 1994 Jul 1;77(7):977-91 PMID: 8020104
  45. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback.
    Chromosoma. 1989 Aug;98(2):81-5 PMID: 2476281
  46. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants.
    Genetics. 1995 Sep;141(1):75-86 PMID: 8536992
  47. Genetic control of chromosome synapsis in yeast meiosis.
    Genome. 1989;31(1):88-94 PMID: 2687110
  48. Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans.
    Genetics. 1993 Jul;134(3):749-68 PMID: 8349107
  49. 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
  50. Roles for two RecA homologs in promoting meiotic chromosome synapsis.
    Genes Dev. 1995 Nov 1;9(21):2684-95 PMID: 7590245
  51. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast.
    J Cell Biol. 1994 Jun;125(6):1191-200 PMID: 8207053
  52. 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
  53. Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene.
    Nucleic Acids Res. 1984 Jul 11;12(13):5495-513 PMID: 6087289
  54. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis.
    Cell. 1998 Aug 7;94(3):387-98 PMID: 9708740
  55. 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
  56. Multiple forms and cellular localization of Drosophila DNA topoisomerase II.
    J Biol Chem. 1986 Jun 15;261(17):8063-9 PMID: 3011806
  57. 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans.
    Nature. 1994 Mar 3;368(6466):32-8 PMID: 7906398
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
1998-09-15
Pages
2932-42
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC317166
Subset
IM
Databases
GENBANK
AF085276
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