Full-Length Synaptonemal Complex Grows Continuously during Meiotic Prophase in Budding Yeast

PLoS Genetics

Volumn 8, Issue 10, 2012, Pages

  Voelkel Meiman, Karen ^a   Moustafa, Sarah S ^a,b   Lefrançois, Philippe ^b   Villeneuve, Anne M ^c   MacQueen, Amy J ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b YALE UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; ESTRADIOL; PROTEIN PCH2; PROTEIN PPH3; PROTEIN ZIP1; PROTEIN ZIP3; UNCLASSIFIED DRUG;

ARTICLE; CELL BUDDING; CELL CYCLE ARREST; CENTROMERE; CHROMOSOME PAIRING; CONTROLLED STUDY; CROSSING OVER; FUNGAL VIABILITY; GENE DOSAGE; GENETIC RECOMBINATION; MEIOTIC PROPHASE I; MOLECULAR DYNAMICS; MUTANT; NONHUMAN; PACHYTENE; POST SYNAPSIS; PROTEIN ASSEMBLY; PROTEIN INCORPORATION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN STRUCTURE; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SPOROGENESIS; STEADY STATE; SYNAPTONEMAL COMPLEX; SYNAPTONEMAL COMPLEX CENTRAL REGION; YEAST CELL;

BIOLOGICAL TRANSPORT; CELL CYCLE CHECKPOINTS; CENTROMERE; CHROMOSOME PAIRING; CHROMOSOMES; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PROPHASE; PROTEIN BINDING; PROTEIN SUBUNITS; SACCHAROMYCETALES; SYNAPTONEMAL COMPLEX;

SACCHAROMYCETALES; SYNAPSIS;

EID: 84868112183     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002993     Document Type: Article

References (47)

1. Bhalla N, Dernburg AF, (2008) Prelude to a division. Annu Rev Cell Dev Biol 24: 397-424.
2. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.
3. Page SL, Hawley RS, (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-558.
4. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and-independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428-2442.
5. MacQueen AJ, Roeder GS, (2009) Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19: 1519-1526.
6. MacQueen AJ, Villeneuve AM, (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674-1687.
7. Zickler D, (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115: 158-174.
8. Zickler D, Lares Ld, Moreau PJF, Leblon F, (1985) Defective pairing and synaptonemal complex formation in a Sordaria mutant (spo44) with a translocated segment of the nucleolar organizer. Chromosoma 92: 37-47.
9. Dong H, Roeder GS, (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148: 417-426.
10. Sym M, Engebrecht J, Roeder GS, (1993) Zip1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
11. Sym M, Roeder GS, (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128: 455-466.
12. Schild-Prufert K, Saito TT, Smolikov S, Gu Y, Hincapie M, et al.(2011) Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. Genetics 189: 411-421.
13. Cheng C-H, Lo Y-H, Liang S-S, Ti S-C, Lin F-M, et al.(2006) SUMO modification control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20: 2067-2081.
14. de Carvalho CE, Colaiacovo MP, (2006) SUMO-related regulation of synaptonemal complex formation during meiosis. Genes Dev 20: 1986.
15. Hooker GW, Roeder GS, (2006) A role for SUMO in meiotic chromosome synapsis. Curr Biol 16: 1238-1243.
16. Agarwal S, Roeder GS, (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
17. Chua PR, Roeder GS, (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
18. Tsubouchi T, Zhao H, Roeder GS, (2006) The meiosis-specific Zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with Zip2. Dev Cell 10: 809-819.
19. Tsubouchi T, Macqueen AJ, Roeder GS, (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217-3226.
20. Roeder GS, (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11: 2600-2621.
21. Martinez-Perez E, Villeneuve AM, (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727-2743.
22. Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, et al.(2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907-919.
23. Novak JE, Ross-Macdonald P, Roeder GS, (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
24. Sym M, Roeder GS, (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79: 283-292.
25. White EJ, Cowan C, Cande WZ, Kaback DB, (2004) In vivo analysis of synaptonemal complex formation during yeast meiosis. Genetics 167: 51-63.
26. Benjamin KR, Zhang C, Shokat KM, Herskowitz I, (2003) Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17: 1524-1539.
27. Jambhekar A, Amon A, (2008) Control of meiosis by respiration. Curr Biol 18: 969-975.
28. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N, (1995) NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 15: 6572-6581.
29. Mitra N, Roeder GS, (2007) A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics 176: 773-787.
30. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327-3332.
31. Falk JE, Chan AC, Hoffmann E, Hochwagen A, (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19: 599-611.
32. Godsel LM, Hobbs RP, Green KJ, (2008) Intermediate filament assembly: dynamics to disease. Trends Cell Biol 18: 28-37.
33. Eriksson JE, He T, Trejo-Skalli AV, Harmala-Brasken AS, Hellman J, et al.(2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117: 919-932.
34. Loidl J, Nairz K, Klein F, (1991) Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100: 221-228.
35. Scherthan H, Wang H, Adelfalk C, White EJ, Cowan C, et al.(2007) Chromosome mobility during meiotic prophase in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104: 16934-16939.
36. Henzel JV, Nabeshima K, Schvarzstein M, Turner BE, Villeneuve AM, et al.(2011) An asymmetric chromosome pair undergoes synaptic adjustment and crossover redistribution during Caenorhabditis elegans meiosis: implications for sex chromosome evolution. Genetics 187: 685-699.
37. Couteau F, Zetka M, (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20: 353-363.
38. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 1127: 29-45.
39. Jessop L, Rockmill B, Roeder GS, Lichten M, (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet 2: e155 doi:10.1371/journal.pgen.0020155.
40. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al.(2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401-415.
41. Fung JC, Rockmill B, Odell M, Roeder GS, (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802.
42. Klutstein M, Xaver M, Shemesh R, Zenvirth D, Klein F, et al.(2009) Separation of roles of Zip1 in meiosis revealed in heterozygous mutants of Saccharomyces cerevisiae. Mol Genet Genomics 282: 453-462.
43. Rockmill B, Engebrecht J, Scherthan H, Loidl J, Roeder GS, (1995) The yeast MER2 gene is required for meiotic recombination and chromosome synapsis. Genetics 141: 49-59.
44. Rockmill B, Roeder GS, (1998) Telomere-mediated chromosome pairing during meiosis in budding yeast. Genes Dev 12: 2574-2586.
45. Sikorski R, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
46. Rockmill B, (2009) Chromosome spreading and immunofluorescence methods in Saccharomyes cerevisiae. Methods Mol Biol 558: 3-13.
47. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual; Nolan C, Ford N, Irwin N, Ferguson M, editors. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.