Home LiteratureArticle Details
PMID: 11731477 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

c(3)G encodes a Drosophila synaptonemal complex protein.

Genes & development ·Vol. 15 ·No. 23 ·2001-12-01 ·Pages 3130-43

Page SL, Hawley RS

Abstract

The meiotic mutant c(3)G (crossover suppressor on 3 of Gowen) abolishes both synaptonemal complex (SC) formation and meiotic recombination, whereas mutations in the mei-W68 and mei-P22 genes prevent recombination but allow normal SC to form. These data, as well as a century of cytogenetic studies, support the argument that meiotic recombination between homologous chromosomes in Drosophila females requires synapsis and SC formation. We have cloned the c(3)G gene and shown that it encodes a protein that is structurally similar to SC proteins from yeast and mammals. Immunolocalization of the C(3)G protein, as well as the analysis of a C(3)G-eGFP expression construct, reveals that C(3)G is present in a thread-like pattern along the lengths of chromosomes in meiotic prophase, consistent with a role as an SC protein present on meiotic bivalents. The availability of a marker for SC in Drosophila allowed the investigation of the extent of synapsis in exchange-defective mutants. These studies indicate that SC formation is impaired in certain meiotic mutants and that the synaptic defect correlates with the exchange defects. Moreover, the observation of interference among the residual exchanges in these mutant oocytes implies that complete SC formation is not required for crossover interference in Drosophila.

MeSH Terms
Animals Cell Nucleus/chemistry,genetics,metabolism Chromosomes/chemistry,genetics,metabolism Cloning, Molecular Drosophila Proteins/chemistry,genetics,metabolism Drosophila melanogaster/genetics Female Genes, Insect/genetics Germ-Line Mutation/genetics Male Meiosis/genetics Microscopy, Fluorescence Models, Molecular Mutation/genetics Nuclear Proteins/chemistry,genetics,metabolism Nucleic Acid Conformation Oocytes/metabolism Ovary/cytology,metabolism Protein Conformation Protein Transport Recombination, Genetic/genetics Synaptonemal Complex/chemistry,genetics Transformation, Genetic
Chemicals
Drosophila Proteins Nuclear Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Page S L
Section of Molecular and Cellular Biology, University of California, Davis, California 95616, USA.
Hawley R S
References (53)
53 references, click to expand
  1. Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis.
    Nat Cell Biol. 1999 Oct;1(6):354-7 PMID: 10559962
  2. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae.
    Cell. 1991 Sep 20;66(6):1239-56 PMID: 1913808
  3. Meiotic chromosomes: integrating structure and function.
    Annu Rev Genet. 1999;33:603-754 PMID: 10690419
  4. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  5. Comparative genomics of the eukaryotes.
    Science. 2000 Mar 24;287(5461):2204-15 PMID: 10731134
  6. A three-dimensional structural dissection of Drosophila polytene chromosomes.
    J Cell Biol. 1995 Oct;131(2):279-95 PMID: 7593159
  7. Identification of double Holliday junctions as intermediates in meiotic recombination.
    Cell. 1995 Dec 1;83(5):783-91 PMID: 8521495
  8. 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
  9. Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis.
    Hum Mol Genet. 1995 Nov;4(11):2007-12 PMID: 8589675
  10. Localization of the N-terminus of SCP1 to the central element of the synaptonemal complex and evidence for direct interactions between the N-termini of SCP1 molecules organized head-to-head.
    Exp Cell Res. 1996 Jul 10;226(1):11-9 PMID: 8660934
  11. Organization of SCP1 protein molecules within synaptonemal complexes of the rat.
    Exp Cell Res. 1996 Jul 10;226(1):20-30 PMID: 8660935
  12. Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9043-8 PMID: 8799151
  13. 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
  14. Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase.
    J Cell Biol. 1997 Apr 7;137(1):5-18 PMID: 9105032
  15. Meiotic chromosomes: it takes two to tango.
    Genes Dev. 1997 Oct 15;11(20):2600-21 PMID: 9334324
  16. Meiotic synapsis in the absence of recombination.
    Science. 1998 Feb 6;279(5352):876-8 PMID: 9452390
  17. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis.
    Cell. 1998 May 1;93(3):349-59 PMID: 9590170
  18. Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae.
    Genetics. 1998 Jun;149(2):817-32 PMID: 9611194
  19. 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
  20. The FlyBase database of the Drosophila Genome Projects and community literature.
    Nucleic Acids Res. 1999 Jan 1;27(1):85-8 PMID: 9847148
  21. Identification of novel Drosophila meiotic genes recovered in a P-element screen.
    Genetics. 1999 Jun;152(2):529-42 PMID: 10353897
  22. The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte.
    Development. 2000 Jul;127(13):2785-94 PMID: 10851125
  23. Hanging on to your homolog: the roles of pairing, synapsis and recombination in the maintenance of homolog adhesion.
    Chromosoma. 2000;109(1-2):3-9 PMID: 10855490
  24. Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila.
    Genetics. 2000 Aug;155(4):1757-72 PMID: 10924472
  25. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins.
    Cell. 2000 Jul 21;102(2):245-55 PMID: 10943844
  26. Genetic control of synaptonemal complexes in Drosophila melanogaster.
    Genetics. 1968 Oct;60(2):335-51 PMID: 5753351
  27. 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
  28. The effects of inversions and the C(3)G mutation on intragenic recombination in Drosophila.
    Genet Res. 1972 Apr;19(2):129-32 PMID: 4624988
  29. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster.
    Genetics. 1972 Jun;71(2):255-86 PMID: 4625747
  30. On recombination-defective meiotic mutants in Drosophila melanogaster.
    Genetics. 1974 Mar;76(3):453-75 PMID: 4208856
  31. Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type.
    Chromosoma. 1975;51(2):157-82 PMID: 806439
  32. Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule--a recombination-associated structure at pachytene?
    Proc Natl Acad Sci U S A. 1975 Aug;72(8):3186-9 PMID: 810799
  33. Synaptonemal complex and recombination nodules in wild-type Drosophila melanogaster females.
    Genetics. 1979 Jun;92(2):511-41 PMID: 114450
  34. Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster.
    Chromosoma. 1979;75(3):259-92 PMID: 119618
  35. 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
  36. Nucleotide sequence of terminal repeats of 412 transposable elements of Drosophila melanogaster. A similarity to proviral long terminal repeats and its implications for the mechanism of transposition.
    J Mol Biol. 1981 Dec 25;153(4):897-915 PMID: 6283088
  37. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference.
    Hereditas. 1982;97(2):179-87 PMID: 6761318
  38. The synaptonemal complex in genetic segregation.
    Annu Rev Genet. 1984;18:331-413 PMID: 6241453
  39. Fluorescence microscopy in three dimensions.
    Methods Cell Biol. 1989;30:353-77 PMID: 2494418
  40. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes.
    EMBO J. 1992 Dec;11(13):5091-100 PMID: 1464329
  41. Yeast genetics and the fall of the classical view of meiosis.
    Cell. 1993 Feb 12;72(3):301-3 PMID: 8431941
  42. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.
    Cell. 1993 Feb 12;72(3):365-78 PMID: 7916652
  43. Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly.
    J Mol Biol. 1993 Mar 20;230(2):436-52 PMID: 7681879
  44. Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis.
    J Cell Biol. 1993 Apr;121(2):241-56 PMID: 8468345
  45. 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
  46. Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex.
    Experientia. 1994 Mar 15;50(3):295-306 PMID: 8143803
  47. An analysis of interference in the fission yeast Schizosaccharomyces pombe.
    Genetics. 1994 Jul;137(3):701-7 PMID: 8088515
  48. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity.
    Genes Dev. 1994 Mar 1;8(5):598-613 PMID: 7523244
  49. Crossover interference is abolished in the absence of a synaptonemal complex protein.
    Cell. 1994 Oct 21;79(2):283-92 PMID: 7954796
  50. Egalitarian and the choice of cell fates in Drosophila melanogaster oogenesis.
    Ciba Found Symp. 1994;182:223-46; discussion 246-54 PMID: 7835153
  51. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction.
    J Cell Sci. 1994 Oct;107 ( Pt 10):2749-60 PMID: 7876343
  52. Predicting coiled coils from protein sequences.
    Science. 1991 May 24;252(5009):1162-4 PMID: 2031185
  53. Organization of the yeast Zip1 protein within the central region of the synaptonemal complex.
    J Cell Biol. 2000 Feb 7;148(3):417-26 PMID: 10662769
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
Published
2001-12-01
Pages
3130-43
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC312841
Subset
IM
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]