The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast

English version České info

During meiosis, homologous chromosomes pair at close proximity to form the synaptonemal complex (SC). This association is mediated by transverse filament proteins that hold the axes of homologous chromosomes together along their entire length. Transverse filament proteins are highly aggregative and can form an aberrant aggregate called the polycomplex that is unassociated with chromosomes. Here, we show that the Ecm11-Gmc2 complex is a novel SC component, functioning to facilitate assembly of the yeast transverse filament protein, Zip1. Ecm11 and Gmc2 initially localize to the synapsis initiation sites, then throughout the synapsed regions of paired homologous chromosomes. The absence of either Ecm11 or Gmc2 substantially compromises the chromosomal assembly of Zip1 as well as polycomplex formation, indicating that the complex is required for extensive Zip1 polymerization. We also show that Ecm11 is SUMOylated in a Gmc2-dependent manner. Remarkably, in the unSUMOylatable ecm11 mutant, assembly of chromosomal Zip1 remained compromised while polycomplex formation became frequent. We propose that the Ecm11-Gmc2 complex facilitates the assembly of Zip1 and that SUMOylation of Ecm11 is critical for ensuring chromosomal assembly of Zip1, thus suppressing polycomplex formation.

Vyšlo v časopise: The Ecm11-Gmc2 Complex Promotes Synaptonemal Complex Formation through Assembly of Transverse Filaments in Budding Yeast. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003194
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003194

Souhrn

Zdroje

1. PetronczkiM, SiomosMF, NasmythK (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112: 423–440.

2. GertonJL, HawleyRS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477–487.

3. SymM, EngebrechtJA, RoederGS (1993) Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365–378.

4. TsubouchiT, RoederGS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308: 870–873.

5. TsubouchiT, MacqueenAJ, RoederGS (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217–3226.

6. ChuaPR, RoederGS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349–359.

7. PerryJ, KlecknerN, BörnerGV (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102: 17594–17599.

8. TsubouchiT, ZhaoH, RoederGS (2006) The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev Cell 10: 809–819.

9. ShinoharaM, OhSD, HunterN, ShinoharaA (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40: 299–309.

10. AgarwalS, RoederGS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245–255.

11. BörnerGV, KlecknerN, HunterN (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29–45.

12. ChenSY, TsubouchiT, RockmillB, SandlerJS, RichardsDR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401–415.

13. AlaniE, PadmoreR, KlecknerN (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419–436.

14. BishopDK, ParkD, XuL, KlecknerN (1992) DMC1: a meiosis-specific yeast homolog of E. coli RecA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439–456.

15. RockmillB, SymM, ScherthanH, RoederGS (1995) Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev 9: 2684–2695.

16. TsubouchiH, RoederGS (2003) The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev Cell 5: 915–925.

17. TsubouchiH, RoederGS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20: 1766–1775.

18. MacqueenAJ, RoederGS (2009) Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19: 1519–1526.

19. FalkJE, ChanAC, HoffmannE, HochwagenA (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19: 599–611.

20. KempB, BoumilRM, StewartMN, DawsonDS (2004) A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18: 1946–1951.

21. GladstoneMN, ObesoD, ChuongH, DawsonDS (2009) The synaptonemal complex protein Zip1 promotes bi-orientation of centromeres at meiosis I. PLoS Genet 5: e1000771 doi:10.1371/journal.pgen.1000771.

22. NewnhamL, JordanP, RockmillB, RoederGS, HoffmannE (2010) The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. Proc Natl Acad Sci U S A 107: 781–785.

23. de CarvalhoCE, ColaiácovoMP (2006) SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev 20: 1986–1992.

24. ChengCH, LoYH, LiangSS, TiSC, LinFM, et al. (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20: 2067–2081.

25. HookerGW, RoederGS (2006) A Role for SUMO in meiotic chromosome synapsis. Curr Biol 16: 1238–1243.

26. EichingerCS, JentschS (2010) Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc Natl Acad Sci U S A 107: 11370–11375.

27. LinFM, LaiYJ, ShenHJ, ChengYH, WangTF (2010) Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 29: 586–596.

28. LussierM, WhiteAM, SheratonJ, di PaoloT, TreadwellJ, et al. (1997) Large scale identification of genes involved in cell surface biosynthesis and architecture in Saccharomyces cerevisiae. Genetics 147: 435–450.

29. ZavecAB, LesnikU, KomelR, CominoA (2004) The Saccharomyces cerevisiae gene ECM11 is a positive effector of meiosis. FEMS Microbiol Lett 241: 193–199.

30. BrarGA, YassourM, FriedmanN, RegevA, IngoliaNT, WeissmanJS (2012) High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335: 552–557.

31. SymM, RoederGS (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128: 455–466.

32. ZavecAB, CominoA, LenassiM, KomelR (2008) Ecm11 protein of yeast Saccharomyces cerevisiae is regulated by sumoylation during meiosis. FEMS Yeast Res 8: 64–70.

33. LakeCM, HawleyRS (2012) The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu Rev Physiol 74: 425–451.

34. CostaY, SpeedR, OllingerR, AlsheimerM, SempleCA, et al. (2005) Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J Cell Sci 118: 2755–2762.

35. Bolcun-FilasE, CostaY, SpeedR, TaggartM, BenaventeR, et al. (2007) SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol 176: 741–747.

36. HamerG, GellK, KouznetsovaA, NovakI, BenaventeR, HöögC (2006) Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 119: 4025–4032.

37. SchrammS, FrauneJ, NaumannR, Hernandez-HernandezA, HöögC, et al. (2011) A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet 7: e1002088 doi:10.1371/journal.pgen.1002088.

38. PageSL, KhetaniRS, LakeCM, NielsenRJ, JeffressJK, et al. (2008) Corona is required for higher-order assembly of transverse filaments into full-length synaptonemal complex in Drosophila oocytes. PLoS Genet 4: e1000194 doi:10.1371/journal.pgen.1000194.

39. RockmillB, RoederGS (1990) Meiosis in asynaptic yeast. Genetics 126: 563–574.

40. JamesP, HalladayJ, CraigEA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425–1436.

41. HunterN, KlecknerN (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59–70.

42. TsubouchiH, RoederGS (2004) The budding yeast Mei5 and Sae3 proteins act together with Dmc1 during meiotic recombination. Genetics 168: 1219–1230.

43. LongtineMS, McKenzieA, DemariniDJ, ShahNG, WachA, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953–961.

44. SchneiderBL, SeufertW, SteinerB, YangQH, FutcherAB (1995) Use of polymerase chain reaction epitope tagging for protein tagging in Saccharomyces cerevisiae. Yeast 11: 1265–1274.

45. StoriciF, LewisLK, ResnickMA (2001) In vivo site-directed mutagenesis using oligonucleotides. Nat Biotechnol 19: 773–776.

46. HudsonJR, DawsonEP, RushingKL, JacksonCH, LockshonD, et al. (1997) The complete set of predicted genes from Saccharomyces cerevisiae in a readily usable form. Genome Res 7: 1169–1173.

47. ChuS, DeRisiJ, EisenM, MulhollandJ, BotsteinD, et al. (1998) The transcriptional program of sporulation in budding yeast. Science 282: 699.

48. PrimigM, WilliamsRM, WinzelerEA, TevzadzeGG, ConwayAR, et al. (2000) The core meiotic transcriptome in budding yeasts. Nat Genet 26: 415–423.

49. SmithAV, RoederGS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136: 957–967.

50. FarmerS, LeungWK, TsubouchiH (2011) Characterization of meiotic recombination initiation sites using pulsed-field gel electrophoresis. Methods Mol Biol 745: 33–45.