Prelude to a Division

Overview

Journal Annu Rev Cell Dev Biol

Publisher Annual Reviews

Specialty Cell Biology

Date 2008 Jul 4

PMID 18597662

Citations 78

Authors

Needhi Bhalla

Abby F Dernburg

Affiliations

Soon will be listed here.

Abstract

Accurate segregation of chromosomes during meiosis requires physical links between homologs. These links are usually established through chromosome pairing, synapsis, and recombination, which occur during meiotic prophase. How chromosomes pair with their homologous partners is one of the outstanding mysteries of meiosis. Surprisingly, experimental evidence indicates that different organisms have found more than one way to accomplish this feat. Whereas some species depend on recombination machinery to achieve homologous pairing, others are able to pair and synapse their homologs in the absence of recombination. To ensure specific pairing between homologous chromosomes, both recombination-dependent and recombination-independent mechanisms must strike the proper balance between forces that promote chromosome interactions and activities that temper the promiscuity of those interactions. The initiation of synapsis is likely to be a tightly regulated step in a process that must be mechanically coupled to homolog pairing.

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References

De Los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth N . The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics. 2003; 164(1):81-94. PMC: 1462551. DOI: 10.1093/genetics/164.1.81. View

Bass H, Marshall W, Sedat J, Agard D, Cande W . Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J Cell Biol. 1997; 137(1):5-18. PMC: 2139864. DOI: 10.1083/jcb.137.1.5. View

Li J, Harper L, Golubovskaya I, Wang C, Weber D, Meeley R . Functional analysis of maize RAD51 in meiosis and double-strand break repair. Genetics. 2007; 176(3):1469-82. PMC: 1931559. DOI: 10.1534/genetics.106.062604. View

Hunter N, Kleckner N . The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell. 2001; 106(1):59-70. DOI: 10.1016/s0092-8674(01)00430-5. View

Chikashige Y, Ding D, Funabiki H, Haraguchi T, Mashiko S, Yanagida M . Telomere-led premeiotic chromosome movement in fission yeast. Science. 1994; 264(5156):270-3. DOI: 10.1126/science.8146661. View

Chaganti R, Schonberg S, German J . A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proc Natl Acad Sci U S A. 1974; 71(11):4508-12. PMC: 433916. DOI: 10.1073/pnas.71.11.4508. View

Schmitt J, Benavente R, Hodzic D, Hoog C, Stewart C, Alsheimer M . Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci U S A. 2007; 104(18):7426-31. PMC: 1863442. DOI: 10.1073/pnas.0609198104. View

Dernburg A, Sedat J, Hawley R . Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell. 1996; 86(1):135-46. DOI: 10.1016/s0092-8674(00)80084-7. View

Tsubouchi T, Roeder G . A synaptonemal complex protein promotes homology-independent centromere coupling. Science. 2005; 308(5723):870-3. DOI: 10.1126/science.1108283. View

10.

Davis L, Smith G . The meiotic bouquet promotes homolog interactions and restricts ectopic recombination in Schizosaccharomyces pombe. Genetics. 2006; 174(1):167-77. PMC: 1569800. DOI: 10.1534/genetics.106.059733. View

11.

Fung J, Rockmill B, Odell M, Roeder G . Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell. 2004; 116(6):795-802. DOI: 10.1016/s0092-8674(04)00249-1. View

12.

Giroux C, Dresser M, Tiano H . Genetic control of chromosome synapsis in yeast meiosis. Genome. 1989; 31(1):88-94. DOI: 10.1139/g89-017. View

13.

Neale M, Keeney S . Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature. 2006; 442(7099):153-8. PMC: 5607947. DOI: 10.1038/nature04885. View

14.

Hooker G, Roeder G . A Role for SUMO in meiotic chromosome synapsis. Curr Biol. 2006; 16(12):1238-43. DOI: 10.1016/j.cub.2006.04.045. View

15.

de Boer E, Dietrich A, Hoog C, Stam P, Heyting C . Meiotic interference among MLH1 foci requires neither an intact axial element structure nor full synapsis. J Cell Sci. 2007; 120(Pt 5):731-6. DOI: 10.1242/jcs.003186. View

16.

Ollinger R, Alsheimer M, Benavente R . Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell. 2004; 16(1):212-7. PMC: 539165. DOI: 10.1091/mbc.e04-09-0771. View

17.

Cromie G, Hyppa R, Taylor A, Zakharyevich K, Hunter N, Smith G . Single Holliday junctions are intermediates of meiotic recombination. Cell. 2006; 127(6):1167-78. PMC: 2803030. DOI: 10.1016/j.cell.2006.09.050. View

18.

Henry J, Camahort R, Rice D, Florens L, Swanson S, Washburn M . Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol Cell Biol. 2006; 26(8):2913-23. PMC: 1446936. DOI: 10.1128/MCB.26.8.2913-2923.2006. View

19.

Nimmo E, Pidoux A, Perry P, Allshire R . Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature. 1998; 392(6678):825-8. DOI: 10.1038/33941. View

20.

Baudat F, Manova K, Yuen J, Jasin M, Keeney S . Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000; 6(5):989-98. DOI: 10.1016/s1097-2765(00)00098-8. View