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Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in , Illuminates a Crossover Assurance Checkpoint


Meiotic recombination, an essential aspect of sexual reproduction, is initiated by programmed DNA double-strand breaks (DSBs). DSBs are catalyzed by the widely-conserved Spo11 enzyme; however, the activity of Spo11 is regulated by additional factors that are poorly conserved through evolution. To expand our understanding of meiotic regulation, we have characterized a novel gene, dsb-1, that is specifically required for meiotic DSB formation in the nematode Caenorhabditis elegans. DSB-1 localizes to chromosomes during early meiotic prophase, coincident with the timing of DSB formation. DSB-1 also promotes normal protein levels and chromosome localization of DSB-2, a paralogous protein that plays a related role in initiating recombination. Mutations that disrupt crossover formation result in prolonged DSB-1 association with chromosomes, suggesting that nuclei may remain in a DSB-permissive state. Extended DSB-1 localization is seen even in mutants with defects in early recombination steps, including spo-11, suggesting that the absence of crossover precursors triggers the extension. Strikingly, failure to form a crossover precursor on a single chromosome pair is sufficient to extend the localization of DSB-1 on all chromosomes in the same nucleus. Based on these observations we propose a model for crossover assurance that acts through DSB-1 to maintain a DSB-permissive state until all chromosome pairs acquire crossover precursors. This work identifies a novel component of the DSB machinery in C. elegans, and sheds light on an important pathway that regulates DSB formation for crossover assurance.


Vyšlo v časopise: Identification of DSB-1, a Protein Required for Initiation of Meiotic Recombination in , Illuminates a Crossover Assurance Checkpoint. PLoS Genet 9(8): e32767. doi:10.1371/journal.pgen.1003679
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003679

Souhrn

Meiotic recombination, an essential aspect of sexual reproduction, is initiated by programmed DNA double-strand breaks (DSBs). DSBs are catalyzed by the widely-conserved Spo11 enzyme; however, the activity of Spo11 is regulated by additional factors that are poorly conserved through evolution. To expand our understanding of meiotic regulation, we have characterized a novel gene, dsb-1, that is specifically required for meiotic DSB formation in the nematode Caenorhabditis elegans. DSB-1 localizes to chromosomes during early meiotic prophase, coincident with the timing of DSB formation. DSB-1 also promotes normal protein levels and chromosome localization of DSB-2, a paralogous protein that plays a related role in initiating recombination. Mutations that disrupt crossover formation result in prolonged DSB-1 association with chromosomes, suggesting that nuclei may remain in a DSB-permissive state. Extended DSB-1 localization is seen even in mutants with defects in early recombination steps, including spo-11, suggesting that the absence of crossover precursors triggers the extension. Strikingly, failure to form a crossover precursor on a single chromosome pair is sufficient to extend the localization of DSB-1 on all chromosomes in the same nucleus. Based on these observations we propose a model for crossover assurance that acts through DSB-1 to maintain a DSB-permissive state until all chromosome pairs acquire crossover precursors. This work identifies a novel component of the DSB machinery in C. elegans, and sheds light on an important pathway that regulates DSB formation for crossover assurance.


Zdroje

1. PageSL, HawleyRS (2003) Chromosome Choreography: The Meiotic Ballet. Science 301: 785–789 doi:10.1126/science.1086605

2. PetronczkiM, SiomosMF, NasmythK (2003) Un Ménage à Quatre: The Molecular Biology of Chromosome Segregation in Meiosis. Cell 112: 423–440 doi:10.1016/S0092-8674(03)00083-7

3. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Current Topics in Developmental Biology. Academic Press, Vol. Volume 52. pp. 1–53. Available: http://www.sciencedirect.com/science/article/pii/S0070215301520086. Accessed 29 September 2012.

4. PadmoreR, CaoL, KlecknerN (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239–1256.

5. CervantesMD, FarahJA, SmithGR (2000) Meiotic DNA Breaks Associated with Recombination in S. pombe. Molecular Cell 5: 883–888 doi:10.1016/S1097-2765(00)80328-7

6. HendersonKA, KeeK, MalekiS, SantiniPA, KeeneyS (2006) Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125: 1321–1332 doi:10.1016/j.cell.2006.04.039

7. SasanumaH, HirotaK, FukudaT, KakushoN, KugouK, et al. (2008) Cdc7-dependent phosphorylation of Mer2 facilitates initiation of yeast meiotic recombination. Genes Dev 22: 398–410 doi:10.1101/gad.1626608

8. WanL, NiuH, FutcherB, ZhangC, ShokatKM, et al. (2008) Cdc28-Clb5 (CDK-S) and Cdc7-Dbf4 (DDK) collaborate to initiate meiotic recombination in yeast. Genes Dev 22: 386–397 doi:10.1101/gad.1626408

9. BordeV, GoldmanAS, LichtenM (2000) Direct coupling between meiotic DNA replication and recombination initiation. Science 290: 806–809.

10. MurakamiH, BordeV, ShibataT, LichtenM, OhtaK (2003) Correlation between premeiotic DNA replication and chromatin transition at yeast recombination initiation sites. Nucleic Acids Res 31: 4085–4090.

11. LangeJ, PanJ, ColeF, ThelenMP, JasinM, et al. (2011) ATM controls meiotic double-strand-break formation. Nature 479: 237–240 doi:10.1038/nature10508

12. JoyceEF, PedersenM, TiongS, White-BrownSK, PaulA, et al. (2011) Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair. J Cell Biol 195: 359–367 doi:10.1083/jcb.201104121

13. ZhangL, KimKP, KlecknerNE, StorlazziA (2011) Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids. PNAS 108: 20036–20041 doi:10.1073/pnas.1117937108

14. CarballoJA, PanizzaS, SerrentinoME, JohnsonAL, GeymonatM, et al. (2013) Budding Yeast ATM/ATR Control Meiotic Double-Strand Break (DSB) Levels by Down-Regulating Rec114, an Essential Component of the DSB-machinery. PLoS Genet 9: e1003545 doi:10.1371/journal.pgen.1003545

15. BergeratA, de MassyB, GadelleD, VaroutasP-C, NicolasA, et al. (1997) An atypical topoisomerase II from archaea with implications for meiotic recombination. Nature 386: 414–417 doi:10.1038/386414a0

16. KeeneyS, GirouxCN, KlecknerN (1997) Meiosis-Specific DNA Double-Strand Breaks Are Catalyzed by Spo11, a Member of a Widely Conserved Protein Family. Cell 88: 375–384 doi:10.1016/S0092-8674(00)81876-0

17. KeeneyS (2008) Spo11 and the Formation of DNA Double-Strand Breaks in Meiosis. Genome Dyn Stab 2: 81–123 doi:__10.1007/7050_2007_026

18. KumarR, BourbonH-M, Massy Bde (2010) Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev 24: 1266–1280 doi:10.1101/gad.571710

19. LiuH, JangJK, KatoN, McKimKS (2002) mei-P22 Encodes a Chromosome-Associated Protein Required for the Initiation of Meiotic Recombination in Drosophila melanogaster. Genetics 162: 245–258.

20. LibbyBJ, ReinholdtLG, SchimentiJC (2003) Positional cloning and characterization of Mei1, a vertebrate-specific gene required for normal meiotic chromosome synapsis in mice. PNAS 100: 15706–15711 doi:10.1073/pnas.2432067100

21. De MuytA, VezonD, GendrotG, GalloisJ-L, StevensR, et al. (2007) AtPRD1 is required for meiotic double strand break formation in Arabidopsis thaliana. EMBO J 26: 4126–4137 doi:10.1038/sj.emboj.7601815

22. De MuytA, PereiraL, VezonD, ChelyshevaL, GendrotG, et al. (2009) A High Throughput Genetic Screen Identifies New Early Meiotic Recombination Functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 doi:10.1371/journal.pgen.1000654

23. DernburgAF, McDonaldK, MoulderG, BarsteadR, DresserM, et al. (1998) Meiotic Recombination in C. elegans Initiates by a Conserved Mechanism and Is Dispensable for Homologous Chromosome Synapsis. Cell 94: 387–398 doi:10.1016/S0092-8674(00)81481-6

24. ChinGM, VilleneuveAM (2001) C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G2 DNA damage checkpoint. Genes Dev 15: 522–534 doi:10.1101/gad.864101

25. HayashiM, ChinGM, VilleneuveAM (2007) C. elegans Germ Cells Switch between Distinct Modes of Double-Strand Break Repair During Meiotic Prophase Progression. PLoS Genet 3: e191 doi:10.1371/journal.pgen.0030191

26. PâquesF, HaberJE (1999) Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349–404.

27. GoodyerW, KaitnaS, CouteauF, WardJD, BoultonSJ, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263–274 doi:10.1016/j.devcel.2007.11.016

28. CouteauF, ZetkaM (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19: 2744–2756 doi:10.1101/gad.1348205

29. Martinez-PerezE, VilleneuveAM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19: 2727–2743 doi:10.1101/gad.1338505

30. CouteauF, NabeshimaK, VilleneuveA, ZetkaM (2004) A Component of C. elegans Meiotic Chromosome Axes at the Interface of Homolog Alignment, Synapsis, Nuclear Reorganization, and Recombination. Current Biology 14: 585–592 doi:10.1016/j.cub.2004.03.033

31. ShinY-H, ChoiY, ErdinSU, YatsenkoSA, KlocM, et al. (2010) Hormad1 Mutation Disrupts Synaptonemal Complex Formation, Recombination, and Chromosome Segregation in Mammalian Meiosis. PLoS Genet 6: e1001190 Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2973818/. Accessed 6 February 2013.

32. DanielK, LangeJ, HachedK, FuJ, AnastassiadisK, et al. (2011) Meiotic homologous chromosome alignment and its surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13: 599–610 doi:10.1038/ncb2213

33. MacQueenAJ, VilleneuveAM (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 15: 1674–1687 doi:10.1101/gad.902601

34. ReddyKC, VilleneuveAM (2004) C. elegans HIM-17 Links Chromatin Modification and Competence for Initiation of Meiotic Recombination. Cell 118: 439–452 doi:10.1016/j.cell.2004.07.026

35. WagnerCR, KuerversL, BaillieDL, YanowitzJL (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467: 839–843 doi:10.1038/nature09429

36. MeneelyPM, McGovernOL, HeinisFI, YanowitzJL (2012) Crossover Distribution and Frequency Are Regulated by him-5 in Caenorhabditis elegans. Genetics 190: 1251–1266 doi:10.1534/genetics.111.137463

37. HodgkinJ, HorvitzHR, BrennerS (1979) Nondisjunction Mutants of the Nematode Caenorhabditis Elegans. Genetics 91: 67–94.

38. KellyKO, DernburgAF, StanfieldGM, VilleneuveAM (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.

39. YokooR, ZawadzkiKA, NabeshimaK, DrakeM, ArurS, et al. (2012) COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers. Cell 149: 75–87 doi:10.1016/j.cell.2012.01.052

40. VilleneuveAM (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136: 887–902.

41. SungP (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241–1243.

42. AlpiA, PasierbekP, GartnerA, LoidlJ (2003) Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112: 6–16 doi:10.1007/s00412-003-0237-5

43. ColaiácovoMP, MacQueenAJ, Martinez-PerezE, McDonaldK, AdamoA, et al. (2003) Synaptonemal Complex Assembly in C. elegans Is Dispensable for Loading Strand-Exchange Proteins but Critical for Proper Completion of Recombination. Developmental Cell 5: 463–474 doi:10.1016/S1534-5807(03)00232-6

44. ThorneLW, ByersB (1993) Stage-specific effects of X-irradiation on yeast meiosis. Genetics 134: 29–42.

45. KimSK, LundJ, KiralyM, DukeK, JiangM, et al. (2001) A gene expression map for Caenorhabditis elegans. Science 293: 2087–2092 doi:10.1126/science.1061603

46. DernburgAF, ZalevskyJ, ColaiácovoMP, VilleneuveAM (2000) Transgene-mediated cosuppression in the C. elegans germ line. Genes Dev 14: 1578–1583 doi:10.1101/gad.14.13.1578

47. RosuS, ZawadzkiKA, StamperEL, LibudaDE, ReeseAL, et al. (co-submitted) The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genetics

48. EcholsN, HarrisonP, BalasubramanianS, LuscombeNM, BertoneP, et al. (2002) Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res 30: 2515–2523.

49. GumiennyTL, LambieE, HartwiegE, HorvitzHR, HengartnerMO (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 126: 1011–1022.

50. BhallaN, DernburgAF (2005) A Conserved Checkpoint Monitors Meiotic Chromosome Synapsis in Caenorhabditis elegans. Science 310: 1683–1686 doi:10.1126/science.1117468

51. KellyWG, SchanerCE, DernburgAF, LeeM-H, KimSK, et al. (2002) X-chromosome silencing in the germline of C. elegans. Development 129: 479–492.

52. SchanerCE, KellyWG (2006) Germline chromatin. WormBook 1–14 doi:10.1895/wormbook.1.73.1

53. PhillipsCM, WongC, BhallaN, CarltonPM, WeiserP, et al. (2005) HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis. Cell 123: 1051–1063 doi:10.1016/j.cell.2005.09.035

54. LorenzA, EstreicherA, KohliJ, LoidlJ (2006) Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 115: 330–340 doi:10.1007/s00412-006-0053-9

55. MoensPB, PearlmanRE, HengHH, TrautW (1998) Chromosome cores and chromatin at meiotic prophase. Curr Top Dev Biol 37: 241–262.

56. ZicklerD, KlecknerN (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603–754 doi:10.1146/annurev.genet.33.1.603

57. BlatY, ProtacioRU, HunterN, KlecknerN (2002) Physical and Functional Interactions among Basic Chromosome Organizational Features Govern Early Steps of Meiotic Chiasma Formation. Cell 111: 791–802 doi:10.1016/S0092-8674(02)01167-4

58. PanizzaS, MendozaMA, BerlingerM, HuangL, NicolasA, et al. (2011) Spo11-Accessory Proteins Link Double-Strand Break Sites to the Chromosome Axis in Early Meiotic Recombination. Cell 146: 372–383 doi:10.1016/j.cell.2011.07.003

59. StorlazziA, TesséS, GarganoS, JamesF, KlecknerN, et al. (2003) Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev 17: 2675–2687 doi:10.1101/gad.275203

60. AroraC, KeeK, MalekiS, KeeneyS (2004) Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13: 549–559.

61. KeeK, ProtacioRU, AroraC, KeeneyS (2004) Spatial organization and dynamics of the association of Rec102 and Rec104 with meiotic chromosomes. EMBO J 23: 1815–1824 doi:10.1038/sj.emboj.7600184

62. LiJ, HookerGW, RoederGS (2006) Saccharomyces cerevisiae Mer2, Mei4 and Rec114 Form a Complex Required for Meiotic Double-Strand Break Formation. Genetics 173: 1969–1981 doi:10.1534/genetics.106.058768

63. MalekiS, NealeM, AroraC, HendersonK, KeeneyS (2007) Interactions between Mei4, Rec114, and other proteins required for meiotic DNA double-strand break formation in Saccharomyces cerevisiae. Chromosoma 116: 471–486 doi:10.1007/s00412-007-0111-y

64. CarltonPM, FarruggioAP, DernburgAF (2006) A Link between Meiotic Prophase Progression and Crossover Control. PLoS Genet 2: e12 doi:10.1371/journal.pgen.0020012

65. MetsDG, MeyerBJ (2009) Condensins Regulate Meiotic DNA Break Distribution, thus Crossover Frequency, by Controlling Chromosome Structure. Cell 139: 73–86 doi:10.1016/j.cell.2009.07.035

66. BhallaN, WynneDJ, JantschV, DernburgAF (2008) ZHP-3 Acts at Crossovers to Couple Meiotic Recombination with Synaptonemal Complex Disassembly and Bivalent Formation in C. elegans. PLoS Genet 4: e1000235 doi:10.1371/journal.pgen.1000235

67. PenknerA, Portik-DobosZ, TangL, SchnabelR, NovatchkovaM, et al. (2007) A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J 26: 5071–5082 doi:10.1038/sj.emboj.7601916

68. MacQueenAJ, ColaiácovoMP, McDonaldK, VilleneuveAM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428–2442 doi:10.1101/gad.1011602

69. WojtaszL, CloutierJM, BaumannM, DanielK, VargaJ, et al. (2012) Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev 26: 958–973 doi:10.1101/gad.187559.112

70. WolteringD, BaumgartnerB, BagchiS, LarkinB, LoidlJ, et al. (2000) Meiotic segregation, synapsis, and recombination checkpoint functions require physical interaction between the chromosomal proteins Red1p and Hop1p. Mol Cell Biol 20: 6646–6658.

71. BailisJM, SmithAV, RoederGS (2000) Bypass of a meiotic checkpoint by overproduction of meiotic chromosomal proteins. Mol Cell Biol 20: 4838–4848.

72. GartnerA, MilsteinS, AhmedS, HodgkinJ, HengartnerMO (2000) A Conserved Checkpoint Pathway Mediates DNA Damage–Induced Apoptosis and Cell Cycle Arrest in C. elegans. Molecular Cell 5: 435–443 doi:10.1016/S1097-2765(00)80438-4

73. GartnerA, BoagPR, BlackwellTK (2008) Germline survival and apoptosis. WormBook 1–20 doi:10.1895/wormbook.1.145.1

74. PhillipsCM, DernburgAF (2006) A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans. Developmental Cell 11: 817–829 doi:10.1016/j.devcel.2006.09.020

75. MacQueenAJ, PhillipsCM, BhallaN, WeiserP, VilleneuveAM, et al. (2005) Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans. Cell 123: 1037–1050 doi:10.1016/j.cell.2005.09.034

76. HayashiM, Mlynarczyk-EvansS, VilleneuveAM (2010) The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis. Genetics 186: 45–58 doi:10.1534/genetics.110.115501

77. SaitoTT, MohideenF, MeyerK, HarperJW, ColaiácovoMP (2012) SLX-1 Is Required for Maintaining Genomic Integrity and Promoting Meiotic Noncrossovers in the Caenorhabditis elegans Germline. PLoS Genet 8: e1002888 doi:10.1371/journal.pgen.1002888

78. HermanRK, KariCK, HartmanPS (1982) Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics 102: 379–400.

79. SchultzJ, RedfieldH (1951) Interchromosomal Effects on Crossing Over in Drosophila. Cold Spring Harb Symp Quant Biol 16: 175–197 doi:10.1101/SQB.1951.016.01.015

80. WoglarA, DaryabeigiA, AdamoA, HabacherC, MachacekT, et al. (2013) Matefin/SUN-1 Phosphorylation Is Part of a Surveillance Mechanism to Coordinate Chromosome Synapsis and Recombination with Meiotic Progression and Chromosome Movement. PLoS Genet 9: e1003335 doi:10.1371/journal.pgen.1003335

81. Lara-GonzalezP, WesthorpeFG, TaylorSS (2012) The Spindle Assembly Checkpoint. Current Biology 22: R966–R980 doi:10.1016/j.cub.2012.10.006

82. AravindL, KooninEV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends in Biochemical Sciences 23: 284–286 doi:10.1016/S0968-0004(98)01257-2

83. RosuS, LibudaDE, VilleneuveAM (2011) Robust Crossover Assurance and Regulated Interhomolog Access Maintain Meiotic Crossover Number. Science 334: 1286–1289 doi:10.1126/science.1212424

84. CohenPE, PollardJW (2001) Regulation of meiotic recombination and prophase I progression in mammals. Bioessays 23: 996–1009 doi:10.1002/bies.1145

85. PenknerAM, FridkinA, GloggnitzerJ, BaudrimontA, MachacekT, et al. (2009) Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1. Cell 139: 920–933 doi:10.1016/j.cell.2009.10.045

86. RichardG-F, KerrestA, LafontaineI, DujonB (2005) Comparative Genomics of Hemiascomycete Yeasts: Genes Involved in DNA Replication, Repair, and Recombination. Mol Biol Evol 22: 1011–1023 doi:10.1093/molbev/msi083

87. KauppiL, JeffreysAJ, KeeneyS (2004) Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 5: 413–424 doi:10.1038/nrg1346

88. PetesTD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2: 360–369 doi:10.1038/35072078

89. BordeV, de MassyB (2013) Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr Opin Genet Dev 23: 147–155 doi:10.1016/j.gde.2012.12.002

90. LichtenM, de MassyB (2011) The Impressionistic Landscape of Meiotic Recombination. Cell 147: 267–270 doi:10.1016/j.cell.2011.09.038

91. MalikS-B, PightlingAW, StefaniakLM, SchurkoAM, LogsdonJMJr (2008) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3: e2879 doi:10.1371/journal.pone.0002879

92. HarperNC, RilloR, Jover-GilS, AssafZJ, BhallaN, et al. (2011) Pairing Centers Recruit a Polo-like Kinase to Orchestrate Meiotic Chromosome Dynamics in C. elegans. Developmental Cell 21: 934–947 doi:10.1016/j.devcel.2011.09.001

93. PhillipsCM, McDonaldKL, DernburgAF (2009) Cytological analysis of meiosis in Caenorhabditis elegans. Methods Mol Biol 558: 171–195 doi:_10.1007/978-1-60761-103-5_11

94. BigelowH, DoitsidouM, SarinS, HobertO (2009) MAQGene: software to facilitate C. elegans mutant genome sequence analysis. Nat Methods 6: 549 doi:10.1038/nmeth.f.260

95. MaduroM, PilgrimD (1995) Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141: 977–988.

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