Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1995 Feb 2;128(4):455–466. doi: 10.1083/jcb.128.4.455

Zip1-induced changes in synaptonemal complex structure and polycomplex assembly

PMCID: PMC2199901  PMID: 7860625

Abstract

The yeast Zip1 protein is a component of the synaptonemal complex (SC), which is an elaborate macromolecular structure found along the lengths of chromosomes during meiosis. Mutations that increase the length of the predicted coiled coil region of the Zip1 protein show that Zip1 influences the width of the SC. Overexpression of the ZIP1 gene results in the formation of two distinct types of higher order structures that are found in the nucleus, but not associated with chromatin. One of these structures resembles the polycomplexes that have been observed in many organisms and are thought to be aggregates of SC components. The second type of structure, which we have termed "networks," does not resemble any previously identified SC-related structure. Assembly of both polycomplexes and networks can occur independently of the Hop1 or Red1 protein, which are thought to be SC components. Our results demonstrate that Zip1 is a structural component of the central region of the SC. More specifically, we speculate that Zip1 is a component of the transverse filaments that lie perpendicular to the long axis of the complex.

Full Text

The Full Text of this article is available as a PDF (3.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  2. Albers K., Fuchs E. The molecular biology of intermediate filament proteins. Int Rev Cytol. 1992;134:243–279. doi: 10.1016/s0074-7696(08)62030-6. [DOI] [PubMed] [Google Scholar]
  3. Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
  4. Chen Q., Pearlman R. E., Moens P. B. Isolation and characterization of a cDNA encoding a synaptonemal complex protein. Biochem Cell Biol. 1992 Oct-Nov;70(10-11):1030–1038. doi: 10.1139/o92-147. [DOI] [PubMed] [Google Scholar]
  5. Dobson M. J., Pearlman R. E., Karaiskakis A., Spyropoulos B., Moens P. B. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci. 1994 Oct;107(Pt 10):2749–2760. doi: 10.1242/jcs.107.10.2749. [DOI] [PubMed] [Google Scholar]
  6. Dresser M. E., Giroux C. N. Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol. 1988 Mar;106(3):567–573. doi: 10.1083/jcb.106.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elledge S. J., Davis R. W. A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae. Gene. 1988 Oct 30;70(2):303–312. doi: 10.1016/0378-1119(88)90202-8. [DOI] [PubMed] [Google Scholar]
  8. Engels F. M., Croes A. F. The synaptinemal complex in yeast. Chromosoma. 1968;25(1):104–106. doi: 10.1007/BF00338237. [DOI] [PubMed] [Google Scholar]
  9. Esponda P. Fine structure of synaptonemal-like complexes in Allium cepa microspores. Protoplasma. 1977;93(1):1–6. doi: 10.1007/BF01276278. [DOI] [PubMed] [Google Scholar]
  10. Fiil A., Moens P. B. The development, structure and function of modified synaptonemal complexes in mosquito oocytes. Chromosoma. 1973;41(1):37–62. doi: 10.1007/BF00284073. [DOI] [PubMed] [Google Scholar]
  11. Goldstein P. Multiple synaptonemal complexes (polycomplexes): origin, structure and function. Cell Biol Int Rep. 1987 Nov;11(11):759–796. doi: 10.1016/0309-1651(87)90157-3. [DOI] [PubMed] [Google Scholar]
  12. Heyting C., Dietrich A. J., Moens P. B., Dettmers R. J., Offenberg H. H., Redeker E. J., Vink A. C. Synaptonemal complex proteins. Genome. 1989;31(1):81–87. doi: 10.1139/g89-016. [DOI] [PubMed] [Google Scholar]
  13. Heyting C., Moens P. B., van Raamsdonk W., Dietrich A. J., Vink A. C., Redeker E. J. Identification of two major components of the lateral elements of synaptonemal complexes of the rat. Eur J Cell Biol. 1987 Feb;43(1):148–154. [PubMed] [Google Scholar]
  14. Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
  15. Hollingsworth N. M., Byers B. HOP1: a yeast meiotic pairing gene. Genetics. 1989 Mar;121(3):445–462. doi: 10.1093/genetics/121.3.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hollingsworth N. M., Goetsch L., Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell. 1990 Apr 6;61(1):73–84. doi: 10.1016/0092-8674(90)90216-2. [DOI] [PubMed] [Google Scholar]
  17. Hollingsworth N. M., Johnson A. D. A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics. 1993 Apr;133(4):785–797. doi: 10.1093/genetics/133.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Horesh O., Simchen G., Friedmann A. Morphogenesis of the synapton during yeast meiosis. Chromosoma. 1979 Oct 2;75(1):101–115. doi: 10.1007/BF00330628. [DOI] [PubMed] [Google Scholar]
  19. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Johnston M., Davis R. W. Sequences that regulate the divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol Cell Biol. 1984 Aug;4(8):1440–1448. doi: 10.1128/mcb.4.8.1440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kilmartin J. V., Dyos S. L., Kershaw D., Finch J. T. A spacer protein in the Saccharomyces cerevisiae spindle poly body whose transcript is cell cycle-regulated. J Cell Biol. 1993 Dec;123(5):1175–1184. doi: 10.1083/jcb.123.5.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Loidl J., Klein F., Scherthan H. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol. 1994 Jun;125(6):1191–1200. doi: 10.1083/jcb.125.6.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Loidl J., Nairz K., Klein F. Meiotic chromosome synapsis in a haploid yeast. Chromosoma. 1991 May;100(4):221–228. doi: 10.1007/BF00344155. [DOI] [PubMed] [Google Scholar]
  24. Meuwissen R. L., Offenberg H. H., Dietrich A. J., Riesewijk A., van Iersel M., Heyting C. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 1992 Dec;11(13):5091–5100. doi: 10.1002/j.1460-2075.1992.tb05616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moens P. B., Heyting C., Dietrich A. J., van Raamsdonk W., Chen Q. Synaptonemal complex antigen location and conservation. J Cell Biol. 1987 Jul;105(1):93–103. doi: 10.1083/jcb.105.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moens P. B., Rapport E. Synaptic structures in the nuclei of sporulating yeast, Saccharomyces cerevisiae (Hansen). J Cell Sci. 1971 Nov;9(3):665–677. doi: 10.1242/jcs.9.3.665. [DOI] [PubMed] [Google Scholar]
  27. Rasmussen S. W. The meotic prophase in Bombyx mori females analyzed by three dimensional reconstructions of synaptonemal complexes. Chromosoma. 1976 Feb 23;54(3):245–293. doi: 10.1007/BF00293453. [DOI] [PubMed] [Google Scholar]
  28. Rockmill B., Roeder G. S. Meiosis in asynaptic yeast. Genetics. 1990 Nov;126(3):563–574. doi: 10.1093/genetics/126.3.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schmekel K., Skoglund U., Daneholt B. The three-dimensional structure of the central region in a synaptonemal complex: a comparison between rat and two insect species, Drosophila melanogaster and Blaps cribrosa. Chromosoma. 1993 Dec;102(10):682–692. doi: 10.1007/BF00650894. [DOI] [PubMed] [Google Scholar]
  30. Schmekel K., Wahrman J., Skoglund U., Daneholt B. The central region of the synaptonemal complex in Blaps cribrosa studied by electron microscope tomography. Chromosoma. 1993 Dec;102(10):669–681. doi: 10.1007/BF00650893. [DOI] [PubMed] [Google Scholar]
  31. Seifert H. S., Chen E. Y., So M., Heffron F. Shuttle mutagenesis: a method of transposon mutagenesis for Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1986 Feb;83(3):735–739. doi: 10.1073/pnas.83.3.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith A., Benavente R. Identification of a structural protein component of rat synaptonemal complexes. Exp Cell Res. 1992 Feb;198(2):291–297. doi: 10.1016/0014-4827(92)90382-i. [DOI] [PubMed] [Google Scholar]
  33. Solari A. J., Moses M. J. The structure of the central region in the synaptonemal complexes of hamster and cricket spermatocytes. J Cell Biol. 1973 Jan;56(1):145–152. doi: 10.1083/jcb.56.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Solari A. J., Vilar O. Multiple complexes in human spermatocytes. Chromosoma. 1978 May 16;66(4):331–340. doi: 10.1007/BF00328533. [DOI] [PubMed] [Google Scholar]
  35. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  36. Steinert P. M., Roop D. R. Molecular and cellular biology of intermediate filaments. Annu Rev Biochem. 1988;57:593–625. doi: 10.1146/annurev.bi.57.070188.003113. [DOI] [PubMed] [Google Scholar]
  37. Stewart M. Intermediate filament structure and assembly. Curr Opin Cell Biol. 1993 Feb;5(1):3–11. doi: 10.1016/s0955-0674(05)80002-x. [DOI] [PubMed] [Google Scholar]
  38. Sym M., Engebrecht J. A., Roeder G. S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 1993 Feb 12;72(3):365–378. doi: 10.1016/0092-8674(93)90114-6. [DOI] [PubMed] [Google Scholar]
  39. Thompson E. A., Roeder G. S. Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast. Mol Gen Genet. 1989 Aug;218(2):293–301. doi: 10.1007/BF00331281. [DOI] [PubMed] [Google Scholar]
  40. Zickler D. Fine structure of chromosome pairing in ten Ascomycetes: meiotic and premeiotic (mitotic) synaptonemal complexes. Chromosoma. 1973;40(4):401–416. doi: 10.1007/BF00399431. [DOI] [PubMed] [Google Scholar]
  41. Zickler D., Olson L. W. The synaptonemal complex and the spindle plaque during meiosis in yeast. Chromosoma. 1975;50(1):1–23. doi: 10.1007/BF00284959. [DOI] [PubMed] [Google Scholar]
  42. von Wettstein D., Rasmussen S. W., Holm P. B. The synaptonemal complex in genetic segregation. Annu Rev Genet. 1984;18:331–413. doi: 10.1146/annurev.ge.18.120184.001555. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES