Meiotic chromosome synapsis in yeast can occur without Spo11-induced DNA double-strand breaks

Genetics

Volumn 168, Issue 2, 2004, Pages 775-783

  Bhuiyan, Hasanuzzaman ^a   Schmekel, Karin ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; PROTEIN; PROTEIN ZIP1; SPO11 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME MARKER; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; DNA STRAND BREAKAGE; DROSOPHILA MELANOGASTER; FUNGAL STRAIN; GAMETE; GENE DELETION; MEIOSIS; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROTEIN FUNCTION; YEAST;

ANIMALS; CHROMOSOME PAIRING; CHROMOSOMES; DNA; DNA DAMAGE; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; ESTERASES; GENETIC MARKERS; MALE; MEIOSIS; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE PROTEINS; SPERMATOCYTES;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 8544278125     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.029660     Document Type: Article

References (43)

1. AGARWAL, S., and G. S. ROEDER, 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
2. BERGERAT, A., B. DE MASSY, D. GADELLE, P. C. VAROUTAS, A. NICOLAS et al., 1997 An atypical topoisomerase 11 from Archaea with implications for meiotic recombination. Nature 386: 414-417.
3. BHUIYAN, H., G. DAHLFORS and K. SCHMEKEL, 2003 Lateral elements inside synaptonemal complex-like polycomplexes in ndt80 mutants of yeast bind DNA. Genetics 163: 539-544.
4. BÖRNER, G. V., N. KLECKNER and N. HUNTER, 2004 Crossover/non- crossover differentiation, synaptonemal complex formation and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
5. BURGESS, S. M., 2002 Homologous chromosome associations and nuclear order in meiotic and mitotically dividing cells of budding yeast. Adv. Genet. 46: 49-90.
6. CAO, L., E. ALANI and N. KLECKNER, 1990 A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089-1101.
7. CHA, R. S., B. M. WEINER, S. KEENEY, J. DEKKER and N. KLECKNER, 2000 Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev. 14: 493-503.
8. DERNBURG, A. F., K. MCDONALD, G. MOULDER, R. BARSTEAD, M. DRESSER et al., 1998 Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
9. FUNG, J. C., W. F. MARSHALL, A. DERNBURG, D. A. AGARD and J. W. SEDAT, 1998 Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol. 141: 5-20.
10. GIROUX, C. N., M. E. DRESSER and H. F. TIANO, 1989 Genetic control of chromosome synapsis in yeast meiosis. Genome 31: 88-94.
11. GUACCI, V., and D. B. KABACK, 1991 Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics 127: 475-488.
12. HENDERSON, K. A., and S. KEENEY, 2004 Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 101: 4519-4524.
13. KEENEY, S., 2001 Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52: 1-53.
14. KEENEY, S., C. N. GIROUX and N. KLECKNER, 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spoil, a member of a widely conserved protein family. Cell 88: 375-384.
15. KLAPHOLZ, S., and R. E. ESPOSITO, 1982 A new mapping method employing a meiotic rec-mutant of yeast. Genetics 100: 387-412.
16. KLAPHOLZ, S., C. S. WADDELL and R. E. ESPOSITO, 1985 The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110: 187-216.
17. LIU, L., S. FRANCO, B. SPYROPOULOS, P. B. MOENS, M. A. BLASCO et al., 2004 Irregular telomeres impair meiotic synapsis and recombination in mice. Proc. Natl. Acad. Sci. USA 101: 6496-6501.
18. LOIDL, J., F. KLEIN and H. SCHERTHAN, 1994 Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125: 1191-1200.
19. LOIDL, J., F. KLEIN and J. ENGEBRECHT, 1998 Genetic and morphological approaches for the analysis of meiotic chromosomes in yeast. Methods Cell Biol. 53: 257-285.
20. MAHADEVAIAH, S. K.,J. M. TURNER, F. BAUDAT, E. P. ROGAKOU, P. DE BOER et al., 2001 Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27: 271-276.
21. MALKOVA, A., F. KLEIN, W.-Y. LEUNG and J. HABER, 2000 HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events Proc. Natl. Acad. Sci. USA 97: 14500-14505.
22. MCKIM, K. S., B. L. GREEN-MARROQUIN, J. J. SEKELSKY, G. CHIN, C. STEINBERG et al., 1998 Meiotic synapsis in the absence of recombination. Science 279: 876-878.
23. NEALE, M. J., M. RAMACHANDRAN, E. TRELLES-STICKEN, H. SCHERTHAN and A. S. GOLDMAN, 2002 Wild-type levels of Spo11-induced DSBs are required for normal single-strand resection during meiosis. Mol. Cell 9: 835-846.
24. NOVAK, J. E., P. B. ROSS-MACDONALD and G. S. ROEDER, 2001 The budding yeast msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
25. PADMORE, R., L. CAO and N. KLECKNER, 1991 Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239-1256.
26. PEOPLES, T. L., E. DEAN, O. GONZALEZ, L. LAMBOURNE and S. M. BURGESS, 2002 Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts. Genes Dev. 16: 1682-1695.
27. RASMUSSEN, S. W., 1976 The meiotic prophase in Bombyx mori females analyzed by three-dimensional reconstructions of synaptonemal complexes. Chromosoma 54: 245-293.
28. ROCKMILL, B., and G. S. ROEDER, 1998 Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev. 12: 2574-2586.
29. ROCKMILL, B., M. SYM, H. SCHERTHAN and G. S. ROEDER, 1995 Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9: 2684-2695.
30. ROEDER, G. S., 1997 Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
31. SCHMEKEL, K., 2000 Methods for immunoelectron microscopic and fine analysis of synaptonemal complexes and nodules in yeast. Chromosoma 109: 110-116.
32. SMITH, A. V., and G. S. ROEDER, 1997 The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136: 957-967.
33. STORLAZZI, A., L. XU, A. SCHWACHA and N. KLECKNER, 1996 Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc. Natl. Acad. Sci. USA 93: 9043-9048.
34. SUN, H., D. TRECO, N. P. SCHULTES and J. W. SZOSTAK, 1989 Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338: 87-90.
35. SYM, M., and G. S. ROEDER, 1995 Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J. Cell Biol. 128: 455-466.
36. SYM, M., J. A. ENGEBRECHT and G. S. ROEDER, 1993 ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
37. THORNE, L. W., and B. BYERS, 1993 Stage-specific effects of X-irradiation on yeast meiosis. Genetics 134: 29-42.
38. TRELLES-STICKEN, E., M. E. DRESSER and H. SCHERTHAN, 2000 Meiotic telomere protein Ndj1p is required for meiosis-distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151: 95-106.
39. TUNG, K.-S., and G. S. ROEDER, 1998 Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149: 817-832.
40. VILLENEUVE, A. M., 1994 A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887-902.
41. WALKER, M. Y., and R. S. HAWLEY, 2000 Hanging on to your homolog: the roles of pairing, synapsis and recombination in the maintenance of homolog adhesion. Chromosoma 109: 3-9.
42. WEINER, B. M., and N. KLECKNER, 1994 Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.
43. XU, L., M. AJIMURA, R. PADMORE, C. KLEIN and N. KLECKNER, 1995 NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 6572-6581.