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Separation of roles of Zip1 in meiosis revealed in heterozygous mutants of Saccharomyces cerevisiae

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Abstract

Synapsis of homologs during meiotic prophase I is associated with a protein complex built along the bivalents—the synaptonemal complex (SC). Mutations in the SC-component gene ZIP1 diminish SC formation, leading to reduced recombination levels and low spore viability. Here we show that in SK1 strains heterozygous for a deletion of ZIP1 in certain regions meiotic interference are impaired with no decrease in recombination levels. The extent of synapsis is over all reduced and NDJ levels of a large endogenous chromosome and of artificial chromosomes (YACs) rise to twice the level of wild type strains. A substantial proportion of mis-segregating YACs had undergone crossing over. This demonstrates that different functions of Zip1 display differential sensitivities to changes in expression levels.

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References

  • Arbel T (1992) Meiotic nondisjunction of homologous chromosomes in the yeast Saccharomyces cerevisiae. PhD Thesis, The Hebrew University of Jerusalem

  • Borner G, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45

    Article  PubMed  Google Scholar 

  • Burke D, Carle G, Olson M (1987) Cloning of large segments of exogenous DNA into yeast by means of artificial chromosome vectors. Science 236:806–812

    Article  PubMed  CAS  Google Scholar 

  • Capieaux E, Ulaszewski S, Balzi E, Goffeau A (1991) Physical, transcriptional and genetical mapping of a 24 kb DNA fragment located between the PMA1 and ATE1 loci on chromosome VII from Saccharomyces cerevisiae. Yeast 7(3):275–280

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, Vader G, Hochwagen A, Roeder GS, Fung JC (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15(3):401–415

    Article  PubMed  CAS  Google Scholar 

  • Guacci V, Kaback D (1991) Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics 127(3):475–488

    PubMed  CAS  Google Scholar 

  • Hugerat Y, Simchen G (1993) Mixed segregation and recombination of chromosomes and YACs during single-division meiosis in spo13 strains of Saccharomyces cerevisiae. Genetics 135:297–308

    PubMed  CAS  Google Scholar 

  • Hugerat Y, Spencer F, Zenvirth D, Simchen G (1994) A versatile method for efficient YAC transfer between any two strains. Genomics 22:108–117

    Article  PubMed  CAS  Google Scholar 

  • Klein S, Zenvirth D, Sherman A, Ried K, Rappold G, Simchen G (1996) Double-strand breaks on YACs during yeast meiosis may reflect meiotic recombination in the human genome. Nat Genet 13:481–484

    Article  PubMed  CAS  Google Scholar 

  • Klieger Y, Yizhar O, Zenvirth D, Shtepel-Milman N, Snoek M, Simchen G (2005) Involvement of Sir2/4 in silencing of DNA breakage and recombination on mouse YACs during yeast meiosis. Mol Biol Cell 16(3):1449–1455

    Article  PubMed  CAS  Google Scholar 

  • Malkova A, Swanson J, German M, McCusker JH, Houseworth EA, Stahl FW, Habe JE (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics 168(1):49–63

    Article  PubMed  CAS  Google Scholar 

  • Page B, Snyder M (1993) Chromosome segregation in yeast. Ann Rev Microbiol 47:231–261

    Article  CAS  Google Scholar 

  • Petronczki M, Siomos M et al (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112(4):423–440

    Article  PubMed  CAS  Google Scholar 

  • Ried K, Mertz A et al (1995) Characterization of a YAC contig spanning the pseudoautosomal region. Genomics 29:787–792

    Article  PubMed  CAS  Google Scholar 

  • Rockmill B, Voelkel-Meiman K et al (2006) Centromere-proximal crossovers are associated with precocious separation of sister chromatids during meiosis in Saccharomyces cerevisiae. Genetics 174(4):1745–1754

    Article  PubMed  Google Scholar 

  • Rothstein R (1991) Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Meth Enzymol 194:281–301

    Article  PubMed  CAS  Google Scholar 

  • Sherman F, Fink GR, Hicks JB (1986) Methods in yeast genetics. Cold Spring Harbor Laboratory pp 163–167

  • Simchen G, Stamberg J (1969) Fine and coarse controls of genetic recombination. Nature 222(5191):329–332

    Article  PubMed  CAS  Google Scholar 

  • Simchen G, Ball N, Nachshon I (1971) Fine control of genetic recombination in yeast. Heredity 26(1):137–140

    Article  PubMed  CAS  Google Scholar 

  • Sym M, Roeder G (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–292

    Article  PubMed  CAS  Google Scholar 

  • Sym M, Roeder G (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128:455–466

    Article  PubMed  CAS  Google Scholar 

  • Sym M, Engebrecht J, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378

    Article  PubMed  CAS  Google Scholar 

  • Tsubouchi T, Roeder G (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308(5723):870–873

    Article  PubMed  CAS  Google Scholar 

  • Tung K, Roeder G (1998) Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149:817–832

    PubMed  CAS  Google Scholar 

  • Zierhut C, Berlinger M, Rupp C, Shinohara A, Klein F (2004) Mnd1 is required for meiotic interhomolog repair. Curr Biol 14:752–762

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Israel Science Foundation (ISF) and the US–Israel Binational Science Foundation (BSF). M. Xaver was supported by grants F3405 and I031-B of the Austrian science foundation.

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Correspondence to Michael Klutstein.

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Communicated by A. Aguilera.

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Klutstein, M., Xaver, M., Shemesh, R. et al. Separation of roles of Zip1 in meiosis revealed in heterozygous mutants of Saccharomyces cerevisiae . Mol Genet Genomics 282, 453–462 (2009). https://doi.org/10.1007/s00438-009-0477-z

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  • DOI: https://doi.org/10.1007/s00438-009-0477-z

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