Home LiteratureArticle Details
PMID: 8647398 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1.

Genetics ·Vol. 141 ·No. 2 ·1995-10-00 ·Pages 619-27

Sekelsky JJ, McKim KS, Chin GM, Hawley RS

Abstract

Meiotic recombination and DNA repair are mediated by overlapping sets of genes. In the yeast Saccharomyces cerevisiae, many genes required to repair DNA double-strand breaks are also required for meiotic recombination. In contrast, mutations in genes required for nucleotide excision repair (NER) have no detectable effects on meiotic recombination in S. cerevisiae. The Drosophila melanogaster mei-9 gene is unique among known recombination genes in that it is required for both meiotic recombination and NER. We have analyzed the mei-9 gene at the molecular level and found that it encodes a homologue of the S. cerevisiae excision repair protein Rad1, the probable homologue of mammalian XPF/ERCC4. Hence, the predominant process of meiotic recombination in Drosophila proceeds through a pathway that is at least partially distinct from that of S. cerevisiae, in that it requires an NER protein. The biochemical properties of the Rad1 protein allow us to explain the observation that mei-9 mutants suppress reciprocal exchange without suppressing the frequency of gene conversion.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Carrier Proteins/genetics DNA Primers DNA Repair/genetics DNA Repair Enzymes DNA Transposable Elements DNA-Binding Proteins Drosophila Proteins Drosophila melanogaster/drug effects,genetics Endonucleases/genetics Fungal Proteins/genetics Genes, Fungal Genes, Insect Meiosis Methyl Methanesulfonate/pharmacology Molecular Sequence Data Mutagenesis Nuclear Proteins Polymerase Chain Reaction Protein Biosynthesis Proteins/chemistry,genetics Receptors, Steroid/metabolism Recombination, Genetic/genetics Saccharomyces cerevisiae/genetics Saccharomyces cerevisiae Proteins Sequence Homology, Amino Acid
Chemicals
Carrier Proteins DNA Primers DNA Transposable Elements DNA-Binding Proteins Drosophila Proteins Fungal Proteins MEI-9 protein, Drosophila Nuclear Proteins Proteins Receptors, Steroid Saccharomyces cerevisiae Proteins Methyl Methanesulfonate Endonucleases RAD1 protein, S cerevisiae DNA Repair Enzymes
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sekelsky J J
Section of Molecular and Cellular Biology, University of California, Davis 95616, USA.
McKim K S
Chin G M
Hawley R S
References (49)
49 references, click to expand
  1. Recombination in ultraviolet-sensitive strains of Saccharomyces cerevisiae.
    Mutat Res. 1968 Nov-Dec;6(3):409-18 PMID: 5728832
  2. Excision repair in Drosophila. Analysis of strand breaks appearing in DNA of mei-9 mutants following mutagen treatment.
    Biochim Biophys Acta. 1980 Nov 14;610(1):116-29 PMID: 6776988
  3. Genetic and molecular characterization of the optomotor-blind gene locus in Drosophila melanogaster.
    Genetics. 1990 Sep;126(1):91-104 PMID: 2121596
  4. Different types of recombination events are controlled by the RAD1 and RAD52 genes of Saccharomyces cerevisiae.
    Genetics. 1988 Oct;120(2):367-77 PMID: 3058548
  5. Meiotic gene conversion mutants in Saccharomyces cerevisiae. I. Isolation and characterization of pms1-1 and pms1-2.
    Genetics. 1985 Aug;110(4):609-46 PMID: 3896926
  6. Isolation and characterization of X-linked mutants of Drosophila melanogaster which are sensitive to mutagens.
    Genetics. 1976 Nov;84(3):485-506 PMID: 187527
  7. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants.
    Nature. 1989 Nov 23;342(6248):396-401 PMID: 2555716
  8. RNA- and single-stranded DNA-binding (SSB) proteins expressed during Drosophila melanogaster oogenesis: a homolog of bacterial and eukaryotic mitochondrial SSBs.
    Gene. 1994 Jun 10;143(2):171-7 PMID: 8206370
  9. The mei-9 alpha mutant of Drosophila melanogaster increases mutagen sensitivity and decreases excision repair.
    Genetics. 1976 Nov;84(3):527-44 PMID: 826452
  10. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease.
    Nature. 1993 Apr 29;362(6423):860-2 PMID: 8479526
  11. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster.
    Genetics. 1972 Jun;71(2):255-86 PMID: 4625747
  12. DNA repair genes and proteins of Saccharomyces cerevisiae.
    Annu Rev Genet. 1993;27:33-70 PMID: 8122907
  13. The Holliday junction on its thirtieth anniversary.
    Genetics. 1994 Oct;138(2):241-6 PMID: 7828807
  14. Genetic control of mutagen sensitivity in Drosophila melanogaster: a new allele at the mei-9 locus on the X-chromosome.
    Mutat Res. 1979 Jan;59(1):129-33 PMID: 107445
  15. Amino acid substitution matrices from protein blocks.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10915-9 PMID: 1438297
  16. Genetic transformation of Drosophila with transposable element vectors.
    Science. 1982 Oct 22;218(4570):348-53 PMID: 6289436
  17. Some of the swi genes of Schizosaccharomyces pombe also have a function in the repair of radiation damage.
    Curr Genet. 1989 Aug;16(2):89-94 PMID: 2598273
  18. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae.
    Genetics. 1994 May;137(1):19-39 PMID: 8056309
  19. Mismatch-specific post-meiotic segregation frequency in yeast suggests a heteroduplex recombination intermediate.
    Nature. 1985 May 23-29;315(6017):350-2 PMID: 3889658
  20. Tests of the double-strand-break repair model for red-mediated recombination of phage lambda and plasmid lambda dv.
    Genetics. 1987 Aug;116(4):501-11 PMID: 2957271
  21. Incision and postincision steps of pyrimidine dimer removal in excision-defective mutants of Saccharomyces cerevisiae.
    J Bacteriol. 1981 Nov;148(2):618-23 PMID: 7028721
  22. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination.
    Mol Cell Biol. 1988 Sep;8(9):3619-26 PMID: 3065620
  23. Timing of molecular events in meiosis in Saccharomyces cerevisiae: stable heteroduplex DNA is formed late in meiotic prophase.
    Mol Cell Biol. 1993 Jan;13(1):373-82 PMID: 8417336
  24. A general model for genetic recombination.
    Proc Natl Acad Sci U S A. 1975 Jan;72(1):358-61 PMID: 1054510
  25. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  26. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  27. Molecular characterization of the human excision repair gene ERCC-1: cDNA cloning and amino acid homology with the yeast DNA repair gene RAD10.
    Cell. 1986 Mar 28;44(6):913-23 PMID: 2420469
  28. Effects of the RAD52 Gene on Recombination in SACCHAROMYCES CEREVISIAE.
    Genetics. 1980 Jan;94(1):31-50 PMID: 17248995
  29. Post-meiotic segregation in strains of Saccharomyces cerevisiae unable to excise pyrimidine dimers.
    Mutat Res. 1976 Oct;37(1):137-40 PMID: 787775
  30. Vectors for P-mediated transformation in Drosophila.
    Biotechnology. 1988;10:437-56 PMID: 2850048
  31. The protein sequence and some intron positions are conserved between the switching gene swi10 of Schizosaccharomyces pombe and the human excision repair gene ERCC1.
    Nucleic Acids Res. 1992 Dec 11;20(23):6347-53 PMID: 1475195
  32. Holliday junctions cleaved by Rad1?
    Nature. 1995 Jan 5;373(6509):27-8 PMID: 7800034
  33. 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
  34. The double-strand-break repair model for recombination.
    Cell. 1983 May;33(1):25-35 PMID: 6380756
  35. Cytogenetic characterization of the 4BC region on the X chromosome of Drosophila melanogaster: localization of the mei-9, norpA and omb genes.
    Chromosoma. 1986;93(4):341-6 PMID: 3084184
  36. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast.
    Genetics. 1980 Jan;94(1):51-68 PMID: 17248996
  37. Co-correction of the ERCC1, ERCC4 and xeroderma pigmentosum group F DNA repair defects in vitro.
    EMBO J. 1993 Sep;12(9):3685-92 PMID: 8253090
  38. It was a very good year for DNA repair.
    Cell. 1994 Jan 14;76(1):1-4 PMID: 8287470
  39. Molecular analysis of recombination events in Drosophila.
    Genetics. 1989 Jul;122(3):653-61 PMID: 2503419
  40. 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
  41. On recombination-defective meiotic mutants in Drosophila melanogaster.
    Genetics. 1974 Mar;76(3):453-75 PMID: 4208856
  42. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75-100 kilobase pairs.
    Chromosoma. 1991 Sep;100(8):487-94 PMID: 1764967
  43. Holliday junction cleavage by yeast Rad1 protein.
    Nature. 1994 Oct 6;371(6497):531-4 PMID: 7935767
  44. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis.
    Cell. 1994 Jan 14;76(1):51-63 PMID: 8287479
  45. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1.
    Science. 1992 Oct 16;258(5081):480-4 PMID: 1411547
  46. Evidence for a repair enzyme complex involving ERCC1 and complementing activities of ERCC4, ERCC11 and xeroderma pigmentosum group F.
    EMBO J. 1993 Sep;12(9):3693-701 PMID: 8253091
  47. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes.
    Mol Cell Biol. 1989 Oct;9(10):4432-40 PMID: 2685551
  48. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Apr;13(4):2324-31 PMID: 8455614
  49. Effects of recombination-deficient and repair-deficient loci on meiotic and mitotic chromosome behavior in Drosophila melanogaster.
    Basic Life Sci. 1980;15:189-208 PMID: 6783029
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
1995-10-00
Pages
619-27
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1206761
Subset
IM
Databases
GENBANK
U27181
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]