Abstract
Caenorhabditis elegans has become a powerful experimental organism with which to study meiotic processes that promote the accurate segregation of chromosomes during the generation of haploid gametes. Haploid reproductive cells are produced through one round of chromosome replication followed by two successive cell divisions. Characteristic meiotic chromosome structure and dynamics are largely conserved in C. elegans. Chromosomes adopt a meiosis-specific structure by loading cohesin proteins, assembling axial elements, and acquiring chromatin marks. Homologous chromosomes pair and form physical connections though synapsis and recombination. Synaptonemal complex and crossover formation allow for the homologs to stably associate prior to remodeling that facilitates their segregation. This chapter will cover conserved meiotic processes as well as highlight aspects of meiosis that are unique to C. elegans.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Adamo A, Montemauri P, Silva N, Ward JD, Boulton SJ, La Volpe A (2008) BRC-1 acts in the inter-sister pathway of meiotic double-strand break repair. EMBO Rep 9(3):287–292
Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102(2):245–255
Albertson DG, Thomson JN (1982) The kinetochores of Caenorhabditis elegans. Chromosoma 86(3):409–428
Alexeev A, Mazin A, Kowalczykowski SC (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat Struct Biol 10(3):182–186
Allard P, Colaiacovo MP (2010) Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc Natl Acad Sci USA 107(47):20405–20410
Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106(1):47–57
Alpi A, Pasierbek P, Gartner A, Loidl J (2003) Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112(1):6–16
Aravind L, Koonin EV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23(8):284–286
Argueso JL, Wanat J, Gemici Z, Alani E (2004) Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168(4):1805–1816
Bai X, Peirson BN, Dong F, Xue C, Makaroff CA (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 11(3):417–430
Bailly AP, Freeman A, Hall J, Declais AC, Alpi A, Lilley DM, Ahmed S, Gartner A (2010) The Caenorhabditis elegans homolog of Gen1/Yen1 resolvases links DNA damage signaling to DNA double-strand break repair. PLoS Genet 6(7):e1001025
Baker BS, Carpenter AT (1972) Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics 71(2):255–286
Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O’Neil NJ, Petalcorin MI, Martin JS, Collis SJ, Cantor SB, Auclair M, Tissenbaum H, West SC, Rose AM, Boulton SJ (2008) RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 135(2):261–271
Bardhan A, Chuong H, Dawson DS (2010) Meiotic cohesin promotes pairing of non-homologous centromeres in early meiotic prophase. Mol Biol Cell 21(11):1799–1809
Barnes TM, Kohara Y, Coulson A, Hekimi S (1995) Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141(1):159–179
Baudat F, de Massy B (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15(5):565–577
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(5):989–998
Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V (2010) Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 6(11):e1001219
Baudrimont A, Penkner A, Woglar A, Mamnun YM, Huliek M, Struck C, Schnabel R, Loidl J, Jantsch V (2011) A new thermosensitive smc-3 allele reveals involvement of cohesin in homologous recombination in C. elegans. PLoS One 6(9):e24799
Bennett RJ, Dunderdale HJ, West SC (1993) Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion. Cell 74(6):1021–1031
Berchowitz LE, Francis KE, Bey AL, Copenhaver GP (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3(8):e132
Bhalla N, Dernburg AF (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310(5754):1683–1686
Bhalla N, Wynne DJ, Jantsch V, Dernburg AF (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4(10):e1000235
Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79(6):1081–1092
Bishop DK, Zickler D (2004) Early decision: meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117(1):9–15
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(6):791–802
Boddy MN, Gaillard PH, McDonald WH, Shanahan P, Yates JR 3rd, Russell P (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107(4):537–548
Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, De Rooij DG, Cooke HJ (2007) SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol 176(6):741–747
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(1):29–45
Boyd JB, Golino MD, Setlow RB (1976) The mei-9 alpha mutant of Drosophila melanogaster increases mutagen sensitivity and decreases excision repair. Genetics 84(3):527–544
Buhler C, Borde V, Lichten M (2007) Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol 5(12):e324
Carpenter AT (1975) Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule—a recombination-associated structure at pachytene? Proc Natl Acad Sci USA 72(8):3186–3189
Cha RS, Weiner BM, Keeney S, Dekker J, Kleckner N (2000) Progression of meiotic DNA replication is modulated by interchromosomal interaction proteins, negatively by Spo11p and positively by Rec8p. Genes Dev 14(4):493–503
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(6943):1002–1009
Chen SY, 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
Chin GM, Villeneuve AM (2001) C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev 15(5):522–534
Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Nasmyth K (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5(2):243–254
Clejan I, Boerckel J, Ahmed S (2006) Developmental modulation of nonhomologous end joining in Caenorhabditis elegans. Genetics 173(3):1301–1317
Colaiacovo MP (2006) The many facets of SC function during C. elegans meiosis. Chromosoma 115(3):195–211
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(3):463–474
Cole F, Keeney S, Jasin M (2010) Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol Cell 39(5):700–710
Copenhaver GP, Housworth EA, Stahl FW (2002) Crossover interference in Arabidopsis. Genetics 160(4):1631–1639
Costa Y, Speed R, Ollinger R, Alsheimer M, Semple CA, Gautier P, Maratou K, Novak I, Hoog C, Benavente R, Cooke HJ (2005) Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J Cell Sci 118(Pt 12):2755–2762
Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19(22):2744–2756
Couteau F, Zetka M (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20(3):353–363
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(7):585–592
Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S (2006) Chromosome territories–a functional nuclear landscape. Curr Opin Cell Biol 18(3):307–316
Crittenden SL, Troemel ER, Evans TC, Kimble J (1994) GLP-1 is localized to the mitotic region of the C. elegans germ line. Development 120(10):2901–2911
Crittenden SL, Leonhard KA, Byrd DT, Kimble J (2006) Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol Biol Cell 17(7):3051–3061
Cromie GA, Rubio CA, Hyppa RW, Smith GR (2005) A natural meiotic DNA break site in Schizosaccharomyces pombe is a hotspot of gene conversion, highly associated with crossing over. Genetics 169(2):595–605
Cromie GA, Hyppa RW, Taylor AF, Zakharyevich K, Hunter N, Smith GR (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell 127(6):1167–1178
Cromie GA, Hyppa RW, Smith GR (2008) The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics 179(3):1157–1167
Curtis D, Clark SH, Chovnick A, Bender W (1989) Molecular analysis of recombination events in Drosophila. Genetics 122(3):653–661
Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, Cooke HJ, Stewart AF, Wassmann K, Jasin M, Keeney S, Toth A (2011) Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13(5):599–610
de Boer E, Stam P, Dietrich AJ, Pastink A, Heyting C (2006) Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci USA 103(25):9607–9612
de Carvalho CE, Zaaijer S, Smolikov S, Gu Y, Schumacher JM, Colaiacovo MP (2008) LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev 22(20):2869–2885
de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM (2003) The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164(1):81–94
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(11):1376–1389
Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86(1):135–146
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(3):387–398
Dernburg AF, Zalevsky J, Colaiacovo MP, Villeneuve AM (2000) Transgene-mediated cosuppression in the C. elegans germ line. Genes Dev 14(13):1578–1583
Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6(3):329–341
Dombecki CR, Chiang AC, Kang HJ, Bilgir C, Stefanski NA, Neva BJ, Klerkx EP, Nabeshima K (2011) The chromodomain protein MRG-1 facilitates the SC-independent homologous pairing during meiosis in Caenorhabditis elegans. Dev Cell 21(6):1092–1103
Dong H, Roeder GS (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148(3):417–426
Duerr JS (2006) Immunohistochemistry. WormBook:1–61
Dumont J, Oegema K, Desai A (2010) A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat Cell Biol 12(9):894–901
Ellermeier C, Smith GR (2005) Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proc Natl Acad Sci USA 102(31):10952–10957
Fan QQ, Petes TD (1996) Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Mol Cell Biol 16(5):2037–2043
Fox PM, Vought VE, Hanazawa M, Lee MH, Maine EM, Schedl T (2011) Cyclin E and CDK-2 regulate proliferative cell fate and cell cycle progression in the C. elegans germline. Development 138(11):2223–2234
Frokjaer-Jensen C, Davis MW, Hollopeter G, Taylor J, Harris TW, Nix P, Lofgren R, Prestgard-Duke M, Bastiani M, Moerman DG, Jorgensen EM (2010) Targeted gene deletions in C. elegans using transposon excision. Nat Methods 7(6):451–453
Garcia-Muse T, Boulton SJ (2007) Meiotic recombination in Caenorhabditis elegans. Chromosome Res 15(5):607–621
Getz TJ, Banse SA, Young LS, Banse AV, Swanson J, Wang GM, Browne BL, Foss HM, Stahl FW (2008) Reduced mismatch repair of heteroduplexes reveals “non”-interfering crossing over in wild-type Saccharomyces cerevisiae. Genetics 178(3):1251–1269
Gillespie PJ, Hirano T (2004) Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts. Curr Biol 14(17):1598–1603
Gillies CB (1975) Synaptonemal complex and chromosome structure. Annu Rev Genet 9:91–109
Giroux CN, Dresser ME, Tiano HF (1989) Genetic-control of chromosome synapsis in yeast meiosis. Genome 31(1):88–94
Goldfarb T, Lichten M (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8(10):e1000520
Goldstein P (1982) The synaptonemal complexes of Caenorhabditis elegans: pachytene karyotype analysis of male and hermaphrodite wild-type and him mutants. Chromosoma 86(4):577–593
Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14(2):263–274
Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20(3):589–600
Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9(4):773–788
Hagstrom KA, Meyer BJ (2003) Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4(7):520–534
Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, Hoog C (2006) Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 119(Pt 19):4025–4032
Harper NC, Rillo R, Jover-Gil S, Assaf ZJ, Bhalla N, Dernburg AF (2011) Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 21(5):934–947
Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, De La Cruz N, Davis P, Duesbury M, Fang R, Fernandes J, Han M, Kishore R, Lee R, Muller HM, Nakamura C, Ozersky P, Petcherski A, Rangarajan A, Rogers A, Schindelman G, Schwarz EM, Tuli MA, Van Auken K, Wang D, Wang X, Williams G, Yook K, Durbin R, Stein LD, Spieth J, Sternberg PW (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res 38(Database issue):D463–D467
Hassold T, Hunt P (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2(4):280–291
Hawley RS, Irick H, Zitron AE, Haddox DA, Lohe A, New C, Whitley MD, Arbel T, Jang J, McKim K et al (1992) There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev Genet 13(6):440–467
Hayashi M, Chin GM, Villeneuve AM (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 3(11):e191
Heidinger-Pauli JM, Unal E, Guacci V, Koshland D (2008) The kleisin subunit of cohesin dictates damage-induced cohesion. Mol Cell 31(1):47–56
Herman RK, Kari CK, Hartman PS (1982) Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics 102(3):379–400
Higgins JD, Armstrong SJ, Franklin FC, Jones GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18(20):2557–2570
Hillers KJ, Villeneuve AM (2003) Chromosome-wide control of meiotic crossing over in C. elegans. Curr Biol 13(18):1641–1647
Hilliker AJ, Chovnick A (1981) Further observations on intragenic recombination in Drosophila melanogaster. Genet Res 38(3):281–296
Hiraoka Y, Ding DQ, Yamamoto A, Tsutsumi C, Chikashige Y (2000) Characterization of fission yeast meiotic mutants based on live observation of meiotic prophase nuclear movement. Chromosoma 109(1–2):103–109
Hirsh D, Oppenheim D, Klass M (1976) Development of the reproductive system of Caenorhabditis elegans. Dev Biol 49(1):200–219
Hodgkin J, Horvitz HR, Brenner S (1979) Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91(1):67–94
Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE (2008) MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet 4(9):e1000186
Holloway JK, Morelli MA, Borst PL, Cohen PE (2010) Mammalian BLM helicase is critical for integrating multiple pathways of meiotic recombination. J Cell Biol 188(6):779–789
Howe M, McDonald KL, Albertson DG, Meyer BJ (2001) HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J Cell Biol 153(6):1227–1238
Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, Bishop DK, Grushcow JM, Brame CJ, Caldwell JA, Hunt DF, Lin R, Smith MM, Allis CD (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102(3):279–291
Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ (2003) Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 13(7):546–553
Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106(1):59–70
Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R, Yoder K, Izumi S, Kuraoka I, Tanaka K, Kimura H, Ikura M, Nishikubo S, Ito T, Muto A, Miyagawa K, Takeda S, Fishel R, Igarashi K, Kamiya K (2007) DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol 27(20):7028–7040
Ip SC, Rass U, Blanco MG, Flynn HR, Skehel JM, West SC (2008) Identification of Holliday junction resolvases from humans and yeast. Nature 456(7220):357–361
Ishiguro T, Tanaka K, Sakuno T, Watanabe Y (2010) Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 12(5):500–506
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(Pt 15):3069–3077
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(18):7998–8006
Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J (2007) Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol 308(1):206–221
Jiang L, Xia M, Strittmatter LI, Makaroff CA (2007) The Arabidopsis cohesin protein SYN3 localizes to the nucleolus and is essential for gametogenesis. Plant J 50(6):1020–1034
Jones GH (1984) The control of chiasma distribution. Symp Soc Exp Biol 38:293–320
Joshi N, Barot A, Jamison C, Borner GV (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5(7):e1000557
Joyce EF, McKim KS (2009) Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics 181(1):39–51
Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M (2002) The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr Biol 12(10):798–812
Kaletta T, Hengartner MO (2006) Finding function in novel targets: C. elegans as a model organism. Nat Rev Drug Discov 5(5):387–398
Karpen GH, Le MH, Le H (1996) Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273(5271):118–122
Katis VL, Lipp JJ, Imre R, Bogdanova A, Okaz E, Habermann B, Mechtler K, Nasmyth K, Zachariae W (2010) Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis. Dev Cell 18(3):397–409
Keeney S (2001) The mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1–53
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(2):617–630
Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, Villeneuve AM, Reinke V (2002) X-chromosome silencing in the germline of C. elegans. Development 129(2):479–492
Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner N (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143(6):924–937
Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427(6974):510–517
Kitajima TS, Sakuno T, Ishiguro K, Iemura S, Natsume T, Kawashima SA, Watanabe Y (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441(7089):46–52
Knoll A, Puchta H (2011) The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. J Exp Bot 62(5):1565–1579
Koszul R, Kleckner N (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19(12):716–724
Koszul R, Kim KP, Prentiss M, Kleckner N, Kameoka S (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133(7):1188–1201
Krejci L, Song B, Bussen W, Rothstein R, Mortensen UH, Sung P (2002) Interaction with Rad51 is indispensable for recombination mediator function of Rad52. J Biol Chem 277(42):40132–40141
Kugou K, Fukuda T, Yamada S, Ito M, Sasanuma H, Mori S, Katou Y, Itoh T, Matsumoto K, Shibata T, Shirahige K, Ohta K (2009) Rec8 guides canonical Spo11 distribution along yeast meiotic chromosomes. Mol Biol Cell 20(13):3064–3076
Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR 3rd, Abmayr SM, Washburn MP, Workman JL (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306(5704):2084–2087
Labella S, Woglar A, Jantsch V, Zetka M (2011) Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev Cell 21(5):948–958
Lachner M, Jenuwein T (2002) The many faces of histone lysine methylation. Curr Opin Cell Biol 14(3):286–298
Lai CH, Chou CY, Ch’ang LY, Liu CS, Lin W (2000) Identification of novel human genes evolutionarily conserved in Caenorhabditis elegans by comparative proteomics. Genome Res 10(5):703–713
Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N (2008) Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell 29(4):517–524
Lee J, Hirano T (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192(2):263–276
Lee MH, Schedl T (2006) RNA in situ hybridization of dissected gonads. WormBook:1–7
Lee J, Iwai T, Yokota T, Yamashita M (2003) Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J Cell Sci 116(Pt 13):2781–2790
Lee J, Kitajima TS, Tanno Y, Yoshida K, Morita T, Miyano T, Miyake M, Watanabe Y (2008) Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat Cell Biol 10(1):42–52
Leung MC, Williams PL, Benedetto A, Au C, Helmcke KJ, Aschner M, Meyer JN (2008) Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 106(1):5–28
Lightfoot J, Testori S, Barroso C, Martinez-Perez E (2011) Loading of meiotic cohesin by SCC-2 is required for processing of DSBs and for the DNA damage checkpoint. Curr Biol 32(17):1421–1430
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(1):11–19
Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung MS, Ercan S, Ikegami K, Jensen M, Kolasinska-Zwierz P, Rosenbaum H, Shin H, Taing S, Takasaki T, Iniguez AL, Desai A, Dernburg AF, Kimura H, Lieb JD, Ahringer J, Strome S, Liu XS (2011) Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res 21(2):227–236
Llano E, Gomez R, Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Vazquez-Quinones L, Hernandez T, de Alava E, Cuadrado A, Barbero JL, Suja JA, Pendas AM (2008) Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice. Genes Dev 22(17):2400–2413
Loidl J (1990) The initiation of meiotic chromosome pairing: the cytological view. Genome 33(6):759–778
Lorenz A, Estreicher A, Kohli J, Loidl J (2006) Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 115(4):330–340
Lorenz A, West SC, Whitby MC (2010) The human Holliday junction resolvase GEN1 rescues the meiotic phenotype of a Schizosaccharomyces pombe mus81 mutant. Nucleic Acids Res 38(6):1866–1873
Lui DY, Peoples-Holst TL, Mell JC, Wu HY, Dean EW, Burgess SM (2006) Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae. Genetics 173(3):1207–1222
MacQueen AJ, Villeneuve AM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15(13):1674–1687
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(18):2428–2442
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(6):1037–1050
Maguire MP (1966) The relationship of crossing over to chromosome synapsis in a short paracentric inversion. Genetics 53(6):1071–1077
Maleki S, Neale MJ, Arora C, Henderson KA, Keeney S (2007) Interactions between Mei4, Rec114, and other proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae. Chromosoma 116(5):471–486
Malone CJ, Misner L, Le Bot N, Tsai MC, Campbell JM, Ahringer J, White JG (2003) The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 115(7):825–836
Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454(7203):479–485
Mannuss A, Dukowic-Schulze S, Suer S, Hartung F, Pacher M, Puchta H (2010) RAD5A, RECQ4A, and MUS81 have specific functions in homologous recombination and define different pathways of DNA repair in Arabidopsis thaliana. Plant Cell 22(10):3318–3330
Marston AL, Tham WH, Shah H, Amon A (2004) A genome-wide screen identifies genes required for centromeric cohesion. Science 303(5662):1367–1370
Martin JS, Winkelmann N, Petalcorin MI, McIlwraith MJ, Boulton SJ (2005) RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol Cell Biol 25(8):3127–3139
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(22):2727–2743
Martinez-Perez E, Schvarzstein M, Barroso C, Lightfoot J, Dernburg AF, Villeneuve AM (2008) Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev 22(20):2886–2901
Martini E, Diaz RL, Hunter N, Keeney S (2006) Crossover homeostasis in yeast meiosis. Cell 126(2):285–295
Mazin AV, Bornarth CJ, Solinger JA, Heyer WD, Kowalczykowski SC (2000) Rad54 protein is targeted to pairing loci by the Rad51 nucleoprotein filament. Mol Cell 6(3):583–592
Mazina OM, Mazin AV (2004) Human Rad54 protein stimulates DNA strand exchange activity of hRad51 protein in the presence of Ca2+. J Biol Chem 279(50):52042–52051
McKee BD (1996) The license to pair: identification of meiotic pairing sites in Drosophila. Chromosoma 105(3):135–141
McKim KS, Howell AM, Rose AM (1988) The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics 120(4):987–1001
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(5352):876–878
McMahill MS, Sham CW, Bishop DK (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5(11):e299
Melby TE, Ciampaglio CN, Briscoe G, Erickson HP (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142(6):1595–1604
Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogue F, Doutriaux MP, Horlow C, Grelon M, Mezard C (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr Biol 15(8):692–701
Mets DG, Meyer BJ (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139(1):73–86
Miki F, Okazaki K, Shimanuki M, Yamamoto A, Hiraoka Y, Niwa O (2002) The 14-kDa dynein light chain-family protein Dlc1 is required for regular oscillatory nuclear movement and efficient recombination during meiotic prophase in fission yeast. Mol Biol Cell 13(3):930–946
Minn IL, Rolls MM, Hanna-Rose W, Malone CJ (2009) SUN-1 and ZYG-12, mediators of centrosome-nucleus attachment, are a functional SUN/KASH pair in Caenorhabditis elegans. Mol Biol Cell 20(21):4586–4595
Monen J, Maddox PS, Hyndman F, Oegema K, Desai A (2005) Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7(12):1248–1255
Moses MJ (1968) Synaptinemal complex. Annu Rev Genet 2:363–412
Motohashi T, Tabara H, Kohara Y (2006) Protocols for large scale in situ hybridization on C. elegans larvae. WormBook:1–8
Muller HJ (1916) The mechanism of crossing over. Am Nat 50:193–221
Munz P (1994) An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137(3):701–707
Nabeshima K, Villeneuve AM, Hillers KJ (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168(3):1275–1292
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(5):683–689
Nag DK, Scherthan H, Rockmill B, Bhargava J, Roeder GS (1995) Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141(1):75–86
Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74:595–648
Nicklas RB (1974) Chromosome segregation mechanisms. Genetics 78(1):205–213
Nottke AC, Beese-Sims SE, Pantelena LF, Reinke V, Shi Y, Colaiacovo MP (2011) SPR-5 is a histone H3K4 demethylase with a role in meiotic double-strand break repair. Proc Natl Acad Sci USA 108(31):12805–12810
Obeso D, Dawson DS (2010) Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLoS One 5(4):e10336
Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, Hunter N (2007) BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130(2):259–272
Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N (2008) RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell 31(3):324–336
Oliveira RA, Nasmyth K (2010) Getting through anaphase: splitting the sisters and beyond. Biochem Soc Trans 38(6):1639–1644
Östergren G (1951) The mechanism of co-orientation in bivalents, and multivalents. Berlingska boktr, Lund
Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15(23):3130–3143
Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525–558
Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, Zhu X, Neale MJ, Jasin M, Socci ND, Hochwagen A, Keeney S (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144(5):719–731
Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, Shirahige K, Klein F (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146(3):372–383
Parisi S, McKay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, Kanaar R, Lehmann E, Hoeijmakers JH, Kohli J (1999) Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol 19(5):3515–3528
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(11):1349–1360
Pasierbek P, Fodermayr M, Jantsch V, Jantsch M, Schweizer D, Loidl J (2003) The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. Exp Cell Res 289(2):245–255
Penkner A, Portik-Dobos Z, Tang L, Schnabel R, Novatchkova M, Jantsch V, Loidl J (2007) A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J 26(24):5071–5082
Penkner AM, Fridkin A, Gloggnitzer J, Baudrimont A, Machacek T, Woglar A, Csaszar E, Pasierbek P, Ammerer G, Gruenbaum Y, Jantsch V (2009) Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 139(5):920–933
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(13):1682–1695
Peoples-Holst TL, Burgess SM (2005) Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev 19(7):863–874
Petalcorin MI, Sandall J, Wigley DB, Boulton SJ (2006) CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. J Mol Biol 361(2):231–242
Petalcorin MI, Galkin VE, Yu X, Egelman EH, Boulton SJ (2007) Stabilization of RAD-51-DNA filaments via an interaction domain in Caenorhabditis elegans BRCA2. Proc Natl Acad Sci USA 104(20):8299–8304
Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2(5):360–369
Phillips CM, Dernburg AF (2006) A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 11(6):817–829
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(6):1051–1063
Phillips CM, McDonald KL, Dernburg AF (2009a) Cytological analysis of meiosis in Caenorhabditis elegans. Methods Mol Biol 558:171–195
Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, Dernburg AF (2009b) Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat Cell Biol 11(8):934–942
Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K (2004) Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 14(4):287–301
Radford SJ, McMahan S, Blanton HL, Sekelsky J (2007) Heteroduplex DNA in meiotic recombination in Drosophila mei-9 mutants. Genetics 176(1):63–72
Rasmussen SW, Holm PB (1984) The synaptonemal complex, recombination nodules and chiasmata in human spermatocytes. Symp Soc Exp Biol 38:271–292
Reddy KC, Villeneuve AM (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118(4):439–452
Riedel CG, Katis VL, Katou Y, Mori S, Itoh T, Helmhart W, Galova M, Petronczki M, Gregan J, Cetin B, Mudrak I, Ogris E, Mechtler K, Pelletier L, Buchholz F, Shirahige K, Nasmyth K (2006) Protein phosphatase 2A protects centromeric sister chromatid cohesion during meiosis I. Nature 441(7089):53–61
Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11(20):2600–2621
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(2):219–229
Rollins RA, Korom M, Aulner N, Martens A, Dorsett D (2004) Drosophila Nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol Cell Biol 24(8):3100–3111
Romano A, Guse A, Krascenicova I, Schnabel H, Schnabel R, Glotzer M (2003) CSC-1: a subunit of the Aurora B kinase complex that binds to the Survivin-like protein BIR-1 and the Incenp-like protein ICP-1. J Cell Biol 161(2):229–236
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(1–2):52–56
Rosenbluth RE, Baillie DL (1981) The genetic analysis of a reciprocal translocation, eT1(III; V), in Caenorhabditis elegans. Genetics 99(3–4):415–428
Rosu S, Libuda DE, Villeneuve AM (2011) Robust crossover assurance and regulated intehomolog access maintain meiotic crossover number. Science 334(6060):1286–1289
Saito TT, Youds JL, Boulton SJ, Colaiacovo MP (2009) Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet 5(11):e1000735
Sanford C, Perry MD (2001) Asymmetrically distributed oligonucleotide repeats in the Caenorhabditis elegans genome sequence that map to regions important for meiotic chromosome segregation. Nucleic Acids Res 29(14):2920–2926
Sato A, Isaac B, Phillips CM, Rillo R, Carlton PM, Wynne DJ, Kasad RA, Dernburg AF (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139(5):907–919
Schild-Prufert K, Saito TT, Smolikov S, Gu Y, Hincapie M, Hill DE, Vidal M, McDonald K, Colaiacovo MP (2011) Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. Genetics 189:411–421
Schlecht HB, Lichten M, Goldman ASH (2004) Compartmentalization of the yeast meiotic nucleus revealed by analysis of ectopic recombination. Genetics 168(3):1189–1203
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(1):20–30
Schramm S, Fraune J, Naumann R, Hernandez-Hernandez A, Hoog C, Cooke HJ, Alsheimer M, Benavente R (2011) A novel mouse synaptonemal complex protein is essential for loading of central element proteins, recombination, and fertility. PLoS Genet 7(5):e1002088
Schumacher JM, Golden A, Donovan PJ (1998) AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J Cell Biol 143(6):1635–1646
Schwacha A, Kleckner N (1994) Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76(1):51–63
Schwartz EK, Heyer WD (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120(2):109–127
Seitan VC, Banks P, Laval S, Majid NA, Dorsett D, Rana A, Smith J, Bateman A, Krpic S, Hostert A, Rollins RA, Erdjument-Bromage H, Tempst P, Benard CY, Hekimi S, Newbury SF, Strachan T (2006) Metazoan Scc4 homologs link sister chromatid cohesion to cell and axon migration guidance. PLoS Biol 4(8):e242
Severson AF, Ling L, van Zuylen V, Meyer BJ (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23(15):1763–1778
Sherwood R, Takahashi TS, Jallepalli PV (2010) Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev 24(24):2723–2731
Shinohara M, Oh SD, Hunter N, Shinohara A (2008) Crossover assurance and crossover interference are distinctly regulated by the ZMM proteins during yeast meiosis. Nat Genet 40(3):299–309
Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472(7343):375–378
Smith GR, Boddy MN, Shanahan P, Russell P (2003) Fission yeast Mus81.Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165(4):2289–2293
Smithies O, Powers PA (1986) Gene conversions and their relation to homologous chromosome pairing. Philos Trans R Soc Lond B Biol Sci 312(1154):291–302
Smolikov S, Eizinger A, Hurlburt A, Rogers E, Villeneuve AM, Colaiacovo MP (2007a) Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 176(4):2027–2033
Smolikov S, Eizinger A, Schild-Prufert K, Hurlburt A, McDonald K, Engebrecht J, Villeneuve AM, Colaiacovo MP (2007b) SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics 176(4):2015–2025
Smolikov S, Schild-Prufert K, Colaiacovo MP (2008) CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis. PLoS Genet 4(6):e1000088
Smolikov S, Schild-Prufert K, Colaiacovo MP (2009) A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet 5(10):e1000669
Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15(3):437–451
Speliotes EK, Uren A, Vaux D, Horvitz HR (2000) The survivin-like C. elegans BIR-1 protein acts with the Aurora-like kinase AIR-2 to affect chromosomes and the spindle midzone. Mol Cell 6(2):211–223
Starr DA, Fridolfsson HN (2010) Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26:421–444
Sugiyama T, New JH, Kowalczykowski SC (1998) DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc Natl Acad Sci USA 95(11):6049–6054
Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64(6):1155–1161
Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72(3):365–378
Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33(1):25–35
Tarsounas M, Morita T, Pearlman RE, Moens PB (1999) RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J Cell Biol 147(2):207–220
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(8):925–934
Thomas SE, McKee BD (2007) Meiotic pairing and disjunction of mini-X chromosomes in Drosophila is mediated by 240-bp rDNA repeats and the homolog conjunction proteins SNM and MNM. Genetics 177(2):785–799
Thomas SE, Soltani-Bejnood M, Roth P, Dorn R, Logsdon JM Jr, McKee BD (2005) Identification of two proteins required for conjunction and regular segregation of achiasmate homologs in Drosophila male meiosis. Cell 123(4):555–568
Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395(6705):854
Tonkin ET, Wang TJ, Lisgo S, Bamshad MJ, Strachan T (2004) NIPBL, encoding a homolog of fungal Scc2-type sister chromatid cohesion proteins and fly Nipped-B, is mutated in Cornelia de Lange syndrome. Nat Genet 36(6):636–641
Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170(2):213–223
Trowbridge K, McKim K, Brill SJ, Sekelsky J (2007) Synthetic lethality of Drosophila in the absence of the MUS81 endonuclease and the DmBlm helicase is associated with elevated apoptosis. Genetics 176(4):1993–2001
Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ (2008) Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev 22(2):194–211
Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308(5723):870–873
Villeneuve AM (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136(3):887–902
Villeneuve AM, Hillers KJ (2001) Whence meiosis? Cell 106(6):647–650
Wagner CR, Kuervers L, Baillie DL, Yanowitz JL (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467(7317):839–843
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(21):7698–7707
Watrin E, Schleiffer A, Tanaka K, Eisenhaber F, Nasmyth K, Peters JM (2006) Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression. Curr Biol 16(9):863–874
Webber HA, Howard L, Bickel SE (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164(6):819–829
Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77(7):977–991
Westergaard M, von Wettstein D (1972) The synaptinemal complex. Annu Rev Genet 6:71–110
Wicky C, Alpi A, Passannante M, Rose A, Gartner A, Muller F (2004) Multiple genetic pathways involving the Caenorhabditis elegans Bloom’s syndrome genes him-6, rad-51, and top-3 are needed to maintain genome stability in the germ line. Mol Cell Biol 24(11):5016–5027
Wignall SM, Villeneuve AM (2009) Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11(7):839–844
Winand NJ, Panzer JA, Kolodner RD (1998) Cloning and characterization of the human and Caenorhabditis elegans homologs of the Saccharomyces cerevisiae MSH5 gene. Genomics 53(1):69–80
Wu HY, Burgess SM (2006) Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16(24):2473–2479
Yildiz O, Majumder S, Kramer B, Sekelsky JJ (2002) Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol Cell 10(6):1503–1509
Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, NJ ON, Rose AM, West SC, Meyer BJ, Boulton SJ (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327(5970):1254–1258
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(3):1271–1283
Zetka M, Rose A (1995) The genetics of meiosis in Caenorhabditis elegans. Trends Genet 11(1):27–31
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(17):2258–2270
Zickler D (1977) Development of the synaptonemal complex and the “recombination nodules” during meiotic prophase in the seven bivalents of the fungus Sordaria macrospora Auersw. Chromosoma 61(4):289–316
Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619–697
Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754
Acknowledgments
We thank Dr. Anne Villeneuve and members of the Colaiácovo lab for early access to unpublished results. We also thank Tim Schedl, Sara Beese-Sims, Takamune Saito, and Patrick Allard for critical reading of this manuscript. This work was supported by National Institutes of Health Grant R01GM072551 (to M.P.C.).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media New York
About this chapter
Cite this chapter
Lui, D.Y., Colaiácovo, M.P. (2013). Meiotic Development in Caenorhabditis elegans . In: Schedl, T. (eds) Germ Cell Development in C. elegans. Advances in Experimental Medicine and Biology, vol 757. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4015-4_6
Download citation
DOI: https://doi.org/10.1007/978-1-4614-4015-4_6
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4614-4014-7
Online ISBN: 978-1-4614-4015-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)