Chromosome pairing and synapsis during Caenorhabditis elegans meiosis

Current Opinion in Cell Biology

Volumn 25, Issue 3, 2013, Pages 349-356

  Rog, Ofer ^a,b   Dernburg, Abby F ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLO LIKE KINASE; RING FINGER PROTEIN; ZINC FINGER PROTEIN;

BINDING SITE; CAENORHABDITIS ELEGANS; CHROMOSOME NUMBER; CHROMOSOME PAIRING; CHROMOSOME REARRANGEMENT; CHROMOSOME SEGREGATION; CHROMOSOME TRANSLOCATION; CONFORMATION; CYTOLOGY; GAMETE; GENETIC ANALYSIS; MEIOSIS; MEIOTIC PROPHASE I; MICROTUBULE; MOLECULAR GENETICS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REPRODUCTION; REVIEW; SISTER CHROMATID; SPERMATOCYTE; SYNAPTONEMAL COMPLEX; TELOMERE; X CHROMOSOME;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMOSOME PAIRING; CHROMOSOMES; MEIOSIS; SYNAPSES;

CAENORHABDITIS ELEGANS; SYNAPSIS;

EID: 84879232999     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.03.003     Document Type: Review

References (72)

1. Hodgkin J., Horvitz H.R., Brenner S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 1979, 91:67-94.
2. Wynne D.J., et al. Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol 2012, 196:47-64.
3. Baudrimont A., et al. Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans. PLoS Genet 2010, 6:e1001219.
4. Merritt C., et al. 3' UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 2008, 18:1476-1482.
5. Frokjaer-Jensen C., et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 2008, 40:1375-1383.
6. Colaiacovo M.P., et al. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 2003, 5:463-474.
7. Phillips C.M., et al. HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 2005, 123:1051-1063.
8. MacQueen A.J., et al. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 2002, 16:2428-2442.
9. Dernburg A.F., et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 1998, 94:387-398.
10. Alpi A., et al. Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 2003, 112:6-16.
11. Penkner A., et al. A conserved function for a Caenorhabditis elegans Com1/Sae2/CtIP protein homolog in meiotic recombination. EMBO J 2007, 26:5071-5082.
12. Hayashi M., Chin G.M., Villeneuve A.M. C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 2007, 3:pe191.
13. MacQueen A.J., et al. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 2005, 123:1037-1050.
14. Albertson D.G., Rose A.M., Villeneuve A.M. Chromosome Organization, Mitosis, and Meiosis. C. elegans II 1997, Cold Spring Harbor Laboratory Press, Cold Spring Harbor (NY), Chapter 3. 2nd edition. D.L. Riddle, T. Blumenthal, B.J. Meyer, J.R. Priess (Eds.).
15. Edgley, M. L. et al. Genetic balancers (April 6, 2006), WormBook, ed. The C. elegans Research Community, WormBook, http://www.wormbook.org/.
16. Phillips C.M., Dernburg A.F. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell 2006, 11:817-829.
17. Phillips C.M., et al. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat Cell Biol 2009, 11:934-942.
18. Hayashi M., Mlynarczyk-Evans S., Villeneuve A.M. The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics 2010, 186:45-58.
19. Sato A., et al. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 2009, 139:907-919.
20. Penkner A., et al. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 2007, 12:873-885.
21. Penkner A.M., et al. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell 2009, 139:920-933.
22. Razafsky D., Hodzic D. Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 2009, 186:461-472.
23. Tapley E.C., Starr D.A. Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr Opin Cell Biol 2013, 25:57-62.
24. Malone C.J., et al. The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell 2003, 115:825-836.
25. Zhou K., et al. A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J Cell Biol 2009, 186:229-241.
26. Harper N.C., et al. Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell 2011, 21:934-947.
27. Nabeshima K., Mlynarczyk-Evans S., Villeneuve A.M. Chromosome painting reveals asynaptic full alignment of homologs and HIM-8-dependent remodeling of X chromosome territories during Caenorhabditis elegans meiosis. PLoS Genet 2011, 7:e1002231.
28. MacQueen A.J., Villeneuve A.M. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev 2001, 15:1674-1687.
29. Labella S., et al. Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev Cell 2011, 21:948-958.
30. Elia A.E., Cantley L.C., Yaffe M.B. Proteomic screen finds pSer/pThr-binding domain localizing Plk1 to mitotic substrates. Science 2003, 299:1228-1231.
31. Hiraoka Y., Dernburg A.F. The SUN rises on meiotic chromosome dynamics. Dev Cell 2009, 17:598-605.
32. Koszul R., et al. Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 2008, 133:1188-1201.
33. Trelles-Sticken E., et al. Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 2005, 170:213-223.
34. Ding D.Q., et al. Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 2004, 6:329-341.
35. Davis L., Smith G.R. The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics 2006, 174:167-177.
36. Tomita K., Cooper J.P. The telomere bouquet controls the meiotic spindle. Cell 2007, 130:113-126.
37. Scherthan H. Telomere attachment and clustering during meiosis. Cell Mol Life Sci 2007, 64:117-124.
38. Lee C.Y., Conrad M.N., Dresser M.E. Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 2012, 8:pe1002730.
39. Zickler D., Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet 1999, 33:603-754.
40. Blat Y., et al. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 2002, 111:791-802.
41. Colaiacovo M.P. The many facets of SC function during C. elegans meiosis. Chromosoma 2006, 115:195-211.
42. Aravind L., Koonin E.V. The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 1998, 23:284-286.
43. Wojtasz L., et al. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 2009, 5:pe1000702.
44. Martinez-Perez E., Villeneuve A.M. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 2005, 19:2727-2743.
45. Couteau F., Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 2005, 19:2744-2756.
46. Goodyer W., et al. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 2008, 14:263-274.
47. Severson A.F., et al. 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 2009, 23:1763-1778.
48. Chin G.M., Villeneuve A.M. 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 2001, 15:522-534.
49. Tzur Y.B., et al. LAB-1 targets PP1 restricts Aurora B, kinase upon entrance into meiosis to promote sister chromatid cohesion. PLoS Biol 2012, 10:e1001378.
50. Couteau F., et al. A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 2004, 14:585-592.
51. Martinez-Perez E., et al. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev 2008, 22:2886-2901.
52. Sym M., Engebrecht J.A., Roeder G.S. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 1993, 72:365-378.
53. Smolikov S., et al. SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics 2007, 176:2015-2025.
54. Smolikov S., Schild-Prufert K., Colaiacovo M.P. 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 2009, 5:e1000669.
55. Schild-Prufert K., et al. Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. Genetics 2011, 189:411-421.
56. Zhang W., et al. HAL-2 promotes homologous pairing during Caenorhabditis elegans meiosis by antagonizing inhibitory effects of synaptonemal complex precursors. PLoS Genet 2012, 8:e1002880.
57. Smolikov S., et al. Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 2007, 176:2027-2033.
58. Xu H., et al. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 2005, 8:949-961.
59. Dombecki C.R., et al. The chromodomain protein MRG-1 facilitates SC-independent homologous pairing during meiosis in Caenorhabditis elegans. Dev Cell 2011, 21:1092-1103.
60. Sommer, R.J. Pristionchus pacificus (August 14, 2006), WormBook, ed. The C. elegans Research Community, WormBook, http://www.wormbook.org/.
61. Henzel J.V., et al. An asymmetric chromosome pair undergoes synaptic adjustment and crossover redistribution during Caenorhabditis elegans meiosis: implications for sex chromosome evolution. Genetics 2011, 187:685-699.
62. Voelkel-Meiman K., et al. Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet 2012, 8:pe1002993.
63. Bhalla N., et al. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 2008, 4:pe1000235.
64. Yokoo R., et al. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 2012, 149:75-87.
65. de Carvalho C.E., et al. LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev 2008, 22:2869-2885.
66. Kleckner N., et al. A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 2004, 101:12592-12597.
67. Rosu S., Libuda D.E., Villeneuve A.M. Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 2011, 334:1286-1289.
68. Youds J.L., et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 2010, 327:1254-1258.
69. Storlazzi A., et al. Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci U S A 1996, 93:9043-9048.
70. Egel-Mitani M., Olson L.W., Egel R. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 1982, 97:179-187.
71. Olson L.W., et al. Asynaptic meiosis in fission yeast?. Hereditas 1978, 89:189-199.
72. Fung J.C., et al. Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 2004, 116:795-802.