The many facets of SC function during C. elegans meiosis

Chromosoma

Volumn 115, Issue 3, 2006, Pages 195-211

  Colaiácovo, Mónica P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; CAENORHABDITIS ELEGANS; CELL DIVISION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; DNA REPLICATION; GAMETE; GENE IDENTIFICATION; GENETIC CONSERVATION; HAPLOIDY; HOMOLOGOUS RECOMBINATION; MEIOSIS; METAPHASE; NONHUMAN; OPEN READING FRAME; PACHYTENE; REVIEW; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY; SYNAPTONEMAL COMPLEX;

ANIMALS; CAENORHABDITIS ELEGANS; MEIOSIS; MODELS, BIOLOGICAL; SYNAPTONEMAL COMPLEX;

CAENORHABDITIS ELEGANS;

EID: 33646026443     PISSN: 00095915     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00412-006-0061-9     Document Type: Review

References (144)

1. Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245-255
2. Albertson DG, Thomson JN (1982) The kinetochores of Caenorhabditis elegans. Chromosoma 86:409-428
3. Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1:15-26
4. Alpi A, Pasierbek P, Gartner A, Loidl J (2003) Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112:6-16
5. Anderson LK, Royer SM, Page SL, McKim KS, Lai A, Lilly MA, Hawley RS (2005) Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc Natl Acad Sci USA 102:4482-4487
6. Aravind L, Koonin EV (1998) The HORMA domain: A common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23:284-286
7. Armstrong SJ, Caryl AP, Jones GH, Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115:3645-3655
8. Barnes TM, Kohara Y, Coulson A, Hekimi S (1995) Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141:159-179
9. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell 6:989-999
10. Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081-1092
11. Bishop DK, Zickler D (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15
12. Blat Y, Protacio RU, Hunter N, Kleckner N (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111:791-802
13. Borner GV, 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
14. Broverman SA, Meneely PM (1994) Meiotic mutants that cause a polar decrease in recombination on the X chromosome in Caenorhabditis elegans. Genetics 136:119-127
15. Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, Nasmyth K (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103:387-398
16. Burgess SM (2002) Homologous chromosome associations and nuclear order in meiotic and mitotically dividing cells of budding yeast. Adv Genet 46:49-90
17. Caryl AP, Armstrong SJ, Jones GH, Franklin FC (2000) A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109:62-71
18. Chan RC, Chan A, Jeon M, Wu TF, Pasqualone D, Rougvie AE, Meyer BJ (2003) Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature 423:1002-1009
19. Cheeseman IM, Desai A (2005) A combined approach for the localization and tandem affinity purification of protein complexes from metazoans. Sci STKE 266:l1
20. Chua PR, Roeder GS (1997) Tam1, a telomere-associated meiotic protein, functions in chromosome synapsis and crossover interference. Genes Dev 11:1786-1800
21. Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:349-359
22. Colaiacovo MP, Stanfield GM, Reddy KC, Reinke V, Kim SK, Villeneuve AM (2002) A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162:113-128
23. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5: 463-474
24. Conrad MN, Dominguez AM, Dresser ME (1997) Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276:1252-1255
25. Cooper JP, Watanabe Y, Nurse P (1998) Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392:828-831
26. Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19:2744-2756
27. Couteau F, Nabeshima K, Villeneuve A, Zetka M (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14:585-592
28. Craig JM, Choo KH (2005) Kiss and break up-safe passage to anaphase in mitosis and meiosis. Chromosoma 114:252-262
29. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376-1389
30. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387-398
31. Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6:329-341
32. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: Occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107:2749-2760
33. 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
34. Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1b and SMC3. J Cell Biol 160:657-670
35. Fawcett DW (1956) The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Biophys Biochem Cytol 2:403-406
36. Fedotova YS, Kolomiets OL, Bogdanov YF (1989) Synaptonemal complex transformations in rye microsporocytes at the diplotene stage of meiosis. Genome 32:816-823
37. Franklin AE, McElver J, Sunjevaric I, Rothstein R, Bowen B, Cande WZ (1999) Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase. Plant Cell 11:809-824
38. 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
39. Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: Diversity amidst conservation. Nat Rev Genet 6:477-487
40. Goldstein P (1982) The synaptonemal complexes of Caenorhabditis elegans: pachytene karyotype analysis of male and hermaphrodite wild-type and him mutants. Chromosoma 86:577-593
41. Goldstein P (1987) Multiple synaptonemal complexes (polycomplexes): origin, structure and function. Cell Biol Int Rep 11:759-796
42. Goldstein P, Slaton DE (1982) The synaptonemal complexes of Caenorhabditis elegans: Comparison of wild-type and mutant strains and pachytene karyotype analysis of wild-type. Chromosoma 84:585-597
43. Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ (2002) The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162:1979-1993
44. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589-600
45. Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126:1011-1022
46. Hassold T, Hunt P (2001) To err (meiotically) is human: The genesis of human aneuploidy. Nat Rev Genet 2:280-291
47. Hawley RS (1980) Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites. Genetics 94:625-646
48. Henderson KA, Keeney S (2005) Synaptonemal complex formation: Where does it start? Bioessays 27:995-998
49. Herman RK, Kari CK, Hartman PS (1982) Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics 102:379-400
50. Herman RK, Kari CK (1989) Recombination between small X chromosome duplications and the X chromosome in Caenorhabditis elegans. Genetics 121:723-737
51. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488-2500
52. Hillers KJ, Villeneuve AM (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 13:1641-1647
53. Hodgkin J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91:67-94
54. Hollingsworth NM, Brill SJ (2004) The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev 18:117-125
55. Hollingsworth NM, Byers B (1989) HOP1: A yeast meiotic pairing gene. Genetics 121:445-462
56. Hollingsworth NM, Goetsch L, Byers B (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61:73-84
57. Hollingsworth NM, Ponte L, Halsey C (1995) MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs in Saccharomyces cerevisiae but not mismatch repair. Genes Dev 9:1728-1739
58. Hunter N (2003) Synaptonemal complexities and commonalities. Mol Cell 12:533-539
59. Jang JK, Sherizen DE, Bhagat R, Manheim EA, McKim KS (2003) Relationship of DNA double-strand breaks to synapsis in Drosophila. J Cell Sci 116:3069-3077
60. Jansen G, Hazendonk E, Thijssen KL, Plasterk RH (1997) Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat Genet 17:119-121
61. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998-8006
62. Jones GH (1987) Chiasmata. In: Moens PB (ed) Meiosis. Academic, Orlando, Florida, pp 213-244
63. Judis L, Chan ER, Schwartz S, Seftel A, Hassold T (2004) Meiosis I arrest and azoospermia in an infertile male explained by failure of formation of a component of the synaptonemal complex. Fertil Steril 81:205-209
64. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231-237
65. Kelly KO, Dernburg AF, Stanfield GM, Villeneuve AM (2000) Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156:617-630
66. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427:510-517
67. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91-103
68. Kohli J, Bahler J (1994) Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex. Experientia 50:295-306
69. Li L, Gerecke EE, Zolan ME (1999) Homolog pairing and meiotic progression in Coprinus cinereus. Chromosoma 108:384-392
70. Liu JG, Yuan L, Brundell E, Bjorkroth B, Daneholt B, Hoog C (1996) 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 226:11-19
71. Liu LX, Spoerke JM, Mulligan EL, Chen J, Reardon B, Westlund B, Sun L, Abel K, Armstrong B, Hardiman G et al (1999) High-throughput isolation of Caenorhabditis elegans deletion mutants. Genome Res 9:859-867
72. Loidl J, Nairz K, Klein F (1991) Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100:221-228
73. MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15:1674-1687
74. 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
75. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037-1050
76. Maguire MP (1986) The pattern of pairing that is effective for crossing over in complex B-A chromosome rearrangements in maize. III. Possible evidence for pairing centers. Chromosoma 94:71-85
77. Marston AL, Amon A (2004) Meiosis: Cell-cycle controls shuffle and deal. Nat Rev Mol Cell Biol 5:983-997
78. 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
79. McKim KS, Howell AM, Rose AM (1988) The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics 120:987-1001
80. McKim KS, Peters K, Rose AM (1993) Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics 134:749-768
81. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, Hawley RS (1998) Meiotic synapsis in the absence of recombination. Science 279:876-878
82. Meneely PM, Farago AF, Kauffman TM (2002) Crossover distribution and high interference for both the X chromosome and an autosome during oogenesis and spermatogenesis in Caenorhabditis elegans. Genetics 162:1169-1177
83. Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11:5091-5100
84. Miyamoto T, Hasuike S, Yogev L, Maduro MR, Ishikawa M, Westphal H, Lamb DJ (2003) Azoospermia in patients heterozygous for a mutation in SYCP3. Lancet 362:1714-1719
85. Miyazaki WY, Orr-Weaver TL (1994) Sister-chromatid cohesion in mitosis and meiosis. Annu Rev Genet 28:167-187
86. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, Heng HH, Spyropoulos B (1997) Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106:207-215
87. Moore DP, Page AW, Tang TT, Kerrebrock AW, Orr-Weaver TL (1998) The cohesion protein MEI-S332 localizes to condensed meiotic and mitotic centromeres until sister chromatids separate. J Cell Biol 140:1003-1012
88. Moses MJ (1956) Chromosomal structures in crayfish spermatocytes. J Biophys Biochem Cytol 2:215-218
89. Munz P (1994) An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137:701-707
90. Nabeshima K, Villeneuve AM, Hillers KJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168:1275-1292
91. Nabeshima K, Villeneuve AM, Colaiacovo MP (2005) Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol 168:683-689
92. Nag DK, Scherthan H, Rockmill B, Bhargava J, Roeder GS (1995) Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141:75-86
93. Nicklas RB (1974) Chromosome segregation mechanisms. Genetics 78:205-213
94. Nimmo ER, Pidoux AL, Perry PE, Allshire RC (1998) Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392:825-828
95. Nonomura KI, Nakano M, Murata K, Miyoshi K, Eiguchi M, Miyao A, Hirochika H, Kurata N (2004) An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis. Mol Genet Genomics 271:121-129
96. Ollinger R, Alsheimer M, Benavente R (2005) Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell 16:212-217
97. Padmore R, Cao L, Kleckner N (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66:1239-1256
98. Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15:3130-3143
99. Page SL, Hawley RS (2003) Chromosome choreography: The meiotic ballet. Science 301:785-789
100. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525-558
101. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15:1349-1360
102. Peoples TL, Dean E, Gonzalez O, Lambourne L, Burgess SM (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
103. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, Meneely PM, Dernburg AF (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123:1051-1063
104. Polanowska J, Martin JS, Fisher R, Scopa T, Rae I, Boulton SJ (2004) Tandem immunoaffinity purification of protein complexes from Caenorhabditis elegans. Biotechniques 36:778-780
105. Reboul J, Vaglio P, Rual JF, Lamesch P, Martinez M, Armstrong CM, Li S, Jacotot L, Bertin N, Janky R et al (2003) C. elegans ORFeome version 1.1: Experimental verification of the genome annotation and resource for proteome-scale protein expression. Nat Genet 34:35-41
106. Reinke V, Smith HE, Nance J, Wang J, Van Doren C, Begley R, Jones SJ, Davis EB, Scherer S, Ward S, Kim SK (2000) A global profile of germline gene expression in C. elegans. Mol Cell 6:605-616
107. Reinke V, Gil IS, Ward S, Kazmer K (2004) Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131:311-323
108. Roeder GS (1997) Meiotic chromosomes: It takes two to tango. Genes Dev 11:2600-2621
109. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157:219-229
110. Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975-987
111. Rose AM, Baillie DL, Curran J (1984) Meiotic pairing behavior of two free duplications of linkage group I in Caenorhabditis elegans. Mol Gen Genet 195:52-56
112. Rosenbluth RE, Baillie DL (1981) The genetic analysis of a reciprocal translocation, eT1(III; V), in Caenorhabditis elegans. Genetics 99:415-428
113. Rosenbluth RE, Johnsen RC, Baillie DL (1990) Pairing for recombination in LGV of Caenorhabditis elegans: A model based on recombination in deficiency heterozygotes. Genetics 124:615-625
114. Ross-Macdonald P, Roeder GS (1994) Mutation of a meiosis-specific MutS homolog decreases crossing over but not mismatch correction. Cell 79:1069-1080
115. Schedl T (1997) Developmental genetics of the germ line. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR (eds) C. elegans II. Cold Spring Harbor, Plainview, New York, pp 241-269
116. Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621-627
117. Schmekel K, Meuwissen RL, Dietrich AJ, Vink AC, van Marle J, van Veen H, Heyting C (1996) Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res 226:20-30
118. Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: Meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90:1123-1135
119. Sherizen D, Jang JK, Bhagat R, Kato N, McKim KS (2005) Meiotic recombination in Drosophila females depends on chromosome continuity between genetically defined boundaries. Genetics 169:767-781
120. Simmer F, Moorman C, Van Der Linden AM, Kuijk E, Van Den Berghe PV, Kamath R, Fraser AG, Ahringer J, Plasterk RH (2003) Genome-wide RNAi of using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 1(1):E12
121. Stack SM (1991) Staining plant cells with silver. II. Chromosome cores. Genome 34:900-908
122. Storlazzi A, Xu L, Schwacha A, Kleckner, N (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
123. Sung P (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241-1243
124. Sym M, Roeder GS (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128:455-466
125. Sym M, Engebrecht JA, Roeder, GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365-378
126. Terasawa M, Shinohara A, Hotta Y, Ogawa H, Ogawa T (1995) Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev 9:925-934
127. Trelles-Sticken E, Dresser ME, Scherthan (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J Cell Biol 151:95-106
128. Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870-873
129. Tung KS, Roeder GS (1998) Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149:817-832
130. Villeneuve AM (1994) A cis -acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136:887-902
131. Villeneuve AM, Hillers KJ (2001) Whence meiosis? Cell 106:647-650
132. von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex and genetic segregation. Annu Rev Genet 18:331-413
133. Walhout AJ, Vidal M (2001) High-throughput yeast two-hybrid assays for large-scale protein interaction mapping. Methods 24:297-306
134. Wan L, de los Santos T, Zhang C, Shokat K, Hollingsworth NM (2004) Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol Biol Cell 15:11-23
135. Wang F, Yoder J, Antoshechkin I, Han M (2003) Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23:7698-7707
136. Webber HA, Howard L, Bickel SE (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164:819-829
137. Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977-991
138. Whetstine JR, Ceron J, Ladd B, Dufourcq P, Reinke V, Shi Y (2005) Regulation of tissue-specific and extracellular matrix-related genes by a class I histone deacetylase. Mol Cell 18:483-490
139. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28:160-164
140. Yuan L, Brundell E, Hoog C (1996) Expression of the meiosis-specific synaptonemal complex protein 1 in a heterologous system results in the formation of large protein structures. Exp Cell Res 229:272-275
141. Zalevsky J, MacQueen AJ, Duffy JB, Kemphues KJ, Villeneuve AM (1999) Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153:1271-1283
142. Zetka MC, Kawasaki I, Strome S, Muller F (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13:2258-2270
143. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619-697
144. Zickler D, Kleckner N (1999) Meiotic chromosomes: Integrating structure and function. Annu Rev Genet 33:603-754