Skip to main content
Genetics logoLink to Genetics
. 1998 Jun;149(2):817–832. doi: 10.1093/genetics/149.2.817

Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae.

K S Tung 1, G S Roeder 1
PMCID: PMC1460213  PMID: 9611194

Abstract

The yeast Zip1 protein (Zip1p) is a component of the central region of the synaptonemal complex (SC). Zip1p is predicted to form a dimer consisting of a coiled-coil domain flanked by globular domains. To analyze the organization of Zip1p within the SC, in-frame deletions of ZIP1 were constructed and analyzed. The results demonstrate that the C terminus but not the N terminus of Zip1p is required for its localization to chromosomes. Deletions in the carboxy half of the predicted coiled-coil region cause decreases in the width of the SC. Based on these results, a model for the organization of Zip1p within the SC is proposed. zip1 deletion mutations were also examined for their effects on sporulation, spore viability, crossing over, and crossover interference. The results demonstrate that the extent of synapsis is positively correlated with the levels of spore viability, crossing over, and crossover interference. In contrast, the role of Zip1p in synapsis is separable from its role in meiotic cell cycle progression. zip1 mutants display interval-specific effects on crossing over.

Full Text

The Full Text of this article is available as a PDF (800.3 KB).

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. Baudat F., Nicolas A. Clustering of meiotic double-strand breaks on yeast chromosome III. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5213–5218. doi: 10.1073/pnas.94.10.5213. [DOI] [PMC free article] [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. Burns N., Grimwade B., Ross-Macdonald P. B., Choi E. Y., Finberg K., Roeder G. S., Snyder M. Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 1994 May 1;8(9):1087–1105. doi: 10.1101/gad.8.9.1087. [DOI] [PubMed] [Google Scholar]
  5. Chua P. R., Roeder G. S. Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev. 1997 Jul 15;11(14):1786–1800. doi: 10.1101/gad.11.14.1786. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Egel R. Synaptonemal complex and crossing-over: structural support or interference? Heredity (Edinb) 1978 Oct;41(2):233–237. doi: 10.1038/hdy.1978.92. [DOI] [PubMed] [Google Scholar]
  9. Goyon C., Lichten M. 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):373–382. doi: 10.1128/mcb.13.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. King J. S., Mortimer R. K. A polymerization model of chiasma interference and corresponding computer simulation. Genetics. 1990 Dec;126(4):1127–1138. doi: 10.1093/genetics/126.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167–8174. doi: 10.1073/pnas.93.16.8167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lichten M., Goldman A. S. Meiotic recombination hotspots. Annu Rev Genet. 1995;29:423–444. doi: 10.1146/annurev.ge.29.120195.002231. [DOI] [PubMed] [Google Scholar]
  14. Liu J. G., Yuan L., Brundell E., Björkroth B., Daneholt B., Hög C. 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):11–19. doi: 10.1006/excr.1996.0197. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Lupas A., Van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 1991 May 24;252(5009):1162–1164. doi: 10.1126/science.252.5009.1162. [DOI] [PubMed] [Google Scholar]
  17. Maguire M. P. Crossover site determination and interference. J Theor Biol. 1988 Oct 21;134(4):565–570. doi: 10.1016/s0022-5193(88)80058-4. [DOI] [PubMed] [Google Scholar]
  18. Meuwissen R. L., Meerts I., Hoovers J. M., Leschot N. J., Heyting C. Human synaptonemal complex protein 1 (SCP1): isolation and characterization of the cDNA and chromosomal localization of the gene. Genomics. 1997 Feb 1;39(3):377–384. doi: 10.1006/geno.1996.4373. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Nag D. K., Petes T. D. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1993 Apr;13(4):2324–2331. doi: 10.1128/mcb.13.4.2324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nag D. K., Scherthan H., Rockmill B., Bhargava J., Roeder G. S. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics. 1995 Sep;141(1):75–86. doi: 10.1093/genetics/141.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Rockmill B., Sym M., Scherthan H., Roeder G. S. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 1995 Nov 1;9(21):2684–2695. doi: 10.1101/gad.9.21.2684. [DOI] [PubMed] [Google Scholar]
  25. Roeder G. S. Sex and the single cell: meiosis in yeast. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10450–10456. doi: 10.1073/pnas.92.23.10450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  27. Sage J., Martin L., Cuzin F., Rassoulzadegan M. cDNA sequence of the murine synaptonemal complex protein 1 (SCP1). Biochim Biophys Acta. 1995 Sep 19;1263(3):258–260. doi: 10.1016/0167-4781(95)00126-2. [DOI] [PubMed] [Google Scholar]
  28. Schmekel K., Daneholt B. The central region of the synaptonemal complex revealed in three dimensions. Trends Cell Biol. 1995 Jun;5(6):239–242. doi: 10.1016/s0962-8924(00)89017-0. [DOI] [PubMed] [Google Scholar]
  29. Schmekel K., Meuwissen R. L., Dietrich A. J., Vink A. C., van Marle J., van Veen H., Heyting C. Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res. 1996 Jul 10;226(1):20–30. doi: 10.1006/excr.1996.0198. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Schwacha A., Kleckner N. 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. doi: 10.1016/0092-8674(94)90172-4. [DOI] [PubMed] [Google Scholar]
  33. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith A. V., Roeder G. S. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol. 1997 Mar 10;136(5):957–967. doi: 10.1083/jcb.136.5.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Snow R. Maximum likelihood estimation of linkage and interference from tetrad data. Genetics. 1979 May;92(1):231–245. doi: 10.1093/genetics/92.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Steinert P. M., Marekov L. N., Fraser R. D., Parry D. A. Keratin intermediate filament structure. Crosslinking studies yield quantitative information on molecular dimensions and mechanism of assembly. J Mol Biol. 1993 Mar 20;230(2):436–452. doi: 10.1006/jmbi.1993.1161. [DOI] [PubMed] [Google Scholar]
  37. Steinert P. M. Organization of coiled-coil molecules in native mouse keratin 1/keratin 10 intermediate filaments: evidence for alternating rows of antiparallel in-register and antiparallel staggered molecules. J Struct Biol. 1991 Oct;107(2):157–174. doi: 10.1016/1047-8477(91)90019-s. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Storlazzi A., Xu L., Schwacha A., Kleckner N. 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):9043–9048. doi: 10.1073/pnas.93.17.9043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Struhl K., Stinchcomb D. T., Scherer S., Davis R. W. High-frequency transformation of yeast: autonomous replication of hybrid DNA molecules. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1035–1039. doi: 10.1073/pnas.76.3.1035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Sym M., Roeder G. S. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell. 1994 Oct 21;79(2):283–292. doi: 10.1016/0092-8674(94)90197-x. [DOI] [PubMed] [Google Scholar]
  43. Sym M., Roeder G. S. Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol. 1995 Feb;128(4):455–466. doi: 10.1083/jcb.128.4.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Säll T., Bengtsson B. O. Apparent negative interference due to variation in recombination frequencies. Genetics. 1989 Aug;122(4):935–942. doi: 10.1093/genetics/122.4.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wu T. C., Lichten M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science. 1994 Jan 28;263(5146):515–518. doi: 10.1126/science.8290959. [DOI] [PubMed] [Google Scholar]
  46. 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 Genetics are provided here courtesy of Oxford University Press

RESOURCES