Skip to main content
Log in

Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis

  • Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Observations of a wide range of organisms show that the centromeres form associations of pairs or small groups at different stages of meiotic prophase. Little is known about the functions or mechanisms of these associations, but in many cases, synaptonemal complex elements seem to play a fundamental role. Two main associations are observed: homology-independent associations very early in the meiotic program—sometimes referred to as centromere coupling—and a later association of homologous centromeres, referred to as centromere pairing or tethering. The later centromere pairing initiates during synaptonemal complex assembly, then persists after the dissolution of the synaptonemal complex. While the function of the homology-independent centromere coupling remains a mystery, centromere pairing appears to have a direct impact on the chromosome segregation fidelity of achiasmatic chromosomes. Recent work in yeast, Drosophila, and mice suggest that centromere pairing is a previously unappreciated, general meiotic feature that may promote meiotic segregation fidelity of the exchange and non-exchange chromosomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245–255

    Article  PubMed  CAS  Google Scholar 

  • Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151:1569–1579

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bardhan A, Chuong H, Dawson DS (2010) Meiotic cohesin promotes pairing of nonhomologous centromeres in early meiotic prophase. Mol Biol Cell 21:1799–1809

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bennett MD (1979) Centromere arrangements in Triticum aestivum and their relationship to synapsis. Heredity 43:157

    Google Scholar 

  • Bhalla N, Dernburg AF (2008) Prelude to a division. Annu Rev Cell Dev Biol 24:397–424

    Article  PubMed  CAS  Google Scholar 

  • Bhalla N, Bhalla N, Wynne DJ, Jantsch V, Dernburg AF, 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:e1000235

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Hoog C, Dawson DS, Pezza RJ (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8:e1002701

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brar GA, Kiburz BM, Zhang Y, Kim JE, White F, Amon A (2006) Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441:532–536

    Article  PubMed  CAS  Google Scholar 

  • Brinkley BR, Brenner SL, Hall JM, Tousson A, Balczon RD, Valdivia MM (1986) Arrangements of kinetochores in mouse cells during meiosis and spermiogenesis. Chromosoma 94:309–317

    Article  PubMed  CAS  Google Scholar 

  • Brown PW, Judis L, Chan ER, Schwartz S, Seftel A, Thomas A, Hassold TJ (2005) Meiotic synapsis proceeds from a limited number of subtelomeric sites in the human male. Am J Hum Genet 77:556–566

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Carlton PM, Cande WZ (2002) Telomeres act autonomously in maize to organize the meiotic bouquet from a semipolarized chromosome orientation. J Cell Biol 157:231–242

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Carpenter AT (1973) A meiotic mutant defective in distributive disjunction in Drosophila melanogaster. Genetics 73:393–428

    PubMed Central  PubMed  CAS  Google Scholar 

  • Chan KL, North PS, Hickson ID (2007) BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 26:3397–3409

    Google Scholar 

  • Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, Yeh CH, Huang HY, Wang TF (2006) SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 20:2067–2081

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cheng EY, Hunt PA, Naluai-Cecchini TA, Fligner CL, Fujimoto VY, Pasternack TL, Schwartz JM, Steinauer JE, Woodruff TJ, Cherry SM et al (2009) Meiotic recombination in human oocytes. PLoS Genet 5:e1000661

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cheslock PS, Kemp BJ, Boumil RM, Dawson DS (2005) The roles of MAD1, MAD2 and MAD3 in meiotic progression and the segregation of nonexchange chromosomes. Nat Genet 37:756–760

    Article  PubMed  CAS  Google Scholar 

  • Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:349–359

    Article  PubMed  CAS  Google Scholar 

  • Church K, Moens PB (1976) Centromere behavior during interphase and meiotic prophase in Allium fistulosum from 3-D, E.M. reconstruction. Chromosoma 56:249–263

    Article  Google Scholar 

  • Clarke L, Carbon J (1983) Genomic substitutions of centromeres in Saccharomyces cerevisiae. Nature 305:23–28

    Article  PubMed  CAS  Google Scholar 

  • Corredor E, Lukaszewski AJ, Pachon P, Allen DC, Naranjo T (2007) Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177:699–706

    Article  PubMed Central  PubMed  Google Scholar 

  • Davis L, Smith GR (2003) Nonrandom homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163:857–874

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dawson DS, Murray AW, Szostak JW (1986) An alternative pathway for meiotic chromosome segregation in yeast. Science 234:713–717

    Article  PubMed  CAS  Google Scholar 

  • de la Fuente R, Parra MT, Viera A, Calvente A, Gomez R, Suja JA, Rufas JS, Page J (2007) Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein. PLoS Genet 3:e198

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135–146

    Article  PubMed  CAS  Google Scholar 

  • Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6:329–341

    Article  PubMed  CAS  Google Scholar 

  • Dong H, Roeder GS (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148:417–426

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Eichinger CS, Jentsch S (2010) Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc Natl Acad Sci U S A 107:11370–11375

    Article  PubMed Central  PubMed  Google Scholar 

  • Falk JE, Chan AC, Hoffmann E, Hochwagen A (2010) A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev Cell 19:599–611

    Article  PubMed  CAS  Google Scholar 

  • Fledel-Alon A, Wilson DJ, Broman K, Wen X, Ober C, Coop G, Przeworski M (2009) Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet 5:e1000658

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gladstone MN, Obeso D, Chuong H, Dawson DS (2009) The synaptonemal complex protein Zip1 promotes bi-orientation of centromeres at meiosis I. PLoS Genet 5:e1000771

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Grell RF (1964) Distributive pairing: the size-dependent mechanism for regular segregation of the fourth chromosomes in Drosophila melanogaster. Proc Natl Acad Sci U S A 52:226–232

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guacci V, Kaback DB (1991) Distributive disjunction of authentic chromosomes in Saccharomyces cerevisiae. Genetics 127:475–488

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hassold T, Hunt PA, Sherman S (1993) Trisomy in humans: incidence, origin and etiology. Curr Opin Genet Dev 3:398–403

    Article  PubMed  CAS  Google Scholar 

  • 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 13:440–467

    Article  PubMed  CAS  Google Scholar 

  • Hayashi A, Ogawa H, Kohno K, Gasser SM, Hiraoka Y (1998) Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells 3:587–601

    Article  PubMed  CAS  Google Scholar 

  • Henderson KA, Keeney S (2005) Synaptonemal complex formation: where does it start? Bioessays 27:995–998

    Article  PubMed  CAS  Google Scholar 

  • Hughes SE, Gilliland WD, Cotitta JL, Takeo S, Collins KA, Hawley RS (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet 5:e1000348

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Humphryes N, Leung WK, Argunhan B, Terentyev Y, Dvorackova M, Tsubouchi H (2013) The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast. PLoS Genet 9:e1003194

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Reports 12:267–275

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jagiello G, Fang JS (1979) Analyses of diplotene chiasma frequencies in mouse oocytes and spermatocytes in relation to ageing and sexual dimorphism. Cytogenet Cell Genet 23:53–60

    Article  PubMed  CAS  Google Scholar 

  • Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J (2004) Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans. Mol Cell Biol 24:7998–8006

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jin Q, Trelles-Sticken E, Scherthan H, Loidl J (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141:21–29

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jordan PW, Karppinen J, Handel MA (2012) Polo-like kinase is required for synaptonemal complex disassembly and phosphorylation in mouse spermatocytes. J Cell Sci 125:5061–5072

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kaback DB, Guacci V, Barber D, Mahon JW (1992) Chromosome size-dependent control of meiotic recombination. Science 256:228–232

    Article  PubMed  CAS  Google Scholar 

  • Karpen GH, Le MH, Le H (1996) Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273:118–122

    Article  PubMed  CAS  Google Scholar 

  • Kemp B, Boumil RM, Stewart MN, Dawson DS (2004) A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18:1946–1951

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103

    Article  PubMed  CAS  Google Scholar 

  • LaFountain JR Jr, Cole RW, Rieder CL (2002) Partner telomeres during anaphase in crane‐fly spermatocytes are connected by an elastic tether that exerts a backward force and resists poleward motion. J Cell Sci 115:1541–1549

    Google Scholar 

  • Lamb NE, Feingold E, Savage A, Avramopoulos D, Freeman S, Gu Y, Hallberg A, Hersey J, Karadima G, Pettay D et al (1997) Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum Mol Genet 6:1391–1399

    Article  PubMed  CAS  Google Scholar 

  • Lee CY, Conrad MN, Dresser ME (2012) Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 8:e1002730

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • LeMaire-Adkins R, Radke K, Hunt PA (1997) Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 139:1611–1619

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li X, Nicklas RB (1995) Mitotic forces control a cell-cycle checkpoint. Nature 373:630–632

    Article  PubMed  CAS  Google Scholar 

  • Lin FM, Lai YJ, Shen HJ, Cheng YH, Wang TF (2010) Yeast axial-element protein, Red1, binds SUMO chains to promote meiotic interhomologue recombination and chromosome synapsis. EMBO J 29:586–596

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu D, Vader G, Vromans MJ, Lampson MA, Lens SM (2009) Sensing chromosome bi-orientation by spatial separation of aurora B kinase from kinetochore substrates. Science 323:1350–1353

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Loidl J, Scherthan H, Kaback DB (1994) Physical association between nonhomologous chromosomes precedes distributive disjunction in yeast. Proc Natl Acad Sci U S A 91:331–334

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Macqueen AJ, Roeder GS (2009) Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol: CB 19:1519–1526

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mann C, Davis RW (1986) Meiotic disjunction of circular minichromosomes in yeast does not require DNA homology. Proc Natl Acad Sci U S A 83:6017–6019

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martinez-Perez E, Shaw P, Reader S, Aragon-Alcaide L, Miller T, Moore G (1999) Homologous chromosome pairing in wheat. J Cell Sci 112(Pt 11):1761–1769

    PubMed  CAS  Google Scholar 

  • Martinez-Perez E, Shaw P, Moore G (2001) The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411:204–207

    Article  PubMed  CAS  Google Scholar 

  • Naranjo T, Corredor E (2008) Nuclear architecture and chromosome dynamics in the search of the pairing partner in meiosis in plants. Cytogenet Genome Res 120:320–330

    Article  PubMed  CAS  Google Scholar 

  • Newnham L, Jordan P, Rockmill B, Roeder GS, Hoffmann E (2010) The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. Proc Natl Acad Sci U S A 107:781–785

    Article  PubMed Central  PubMed  Google Scholar 

  • Nicklas RB, Koch CA (1969) Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes. J Cell Biol 43:40–50

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Obeso D, Dawson DS (2010) Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLoS ONE 5:e10336

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Oliver TR, Feingold E, Yu K, Cheung V, Tinker S, Yadav-Shah M, Masse N, Sherman SL (2008) New insights into human nondisjunction of chromosome 21 in oocytes. PLoS Genet 4:e1000033

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Östergren G (1951) The mechanism of co-orientation in bivalents and multivalents. Hereditas 37:85–156

    Article  Google Scholar 

  • Page J, Viera A, Parra MT, de la Fuente R, Suja JA, Prieto I, Barbero JL, Rufas JS, Berrios S, Fernandez-Donoso R (2006) Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet 2:e136

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Phillips D, Nibau C, Wnetrzak J, Jenkins G (2012) High resolution analysis of meiotic chromosome structure and behaviour in barley (Hordeum vulgare L.). PLoS One 7:e39539

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Prieto P, Santos AP, Moore G, Shaw P (2004) Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma 112:300–307

    Article  PubMed  Google Scholar 

  • Qiao H, Chen JK, Reynolds A, Hoog C, Paddy M, Hunter N (2012) Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLoS Genet 8:e1002790

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rasmussen SW (1977) The transformation of the synaptonemal complex into the ‘elimination chromatin’ in Bombyx mori oocytes. Chromosoma 60:205–221

    Article  PubMed  CAS  Google Scholar 

  • Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat F, de Massy B, Wang J et al (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45:269–278

    Article  PubMed  CAS  Google Scholar 

  • Ronceret A, Doutriaux MP, Golubovskaya IN, Pawlowski WP (2009) PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. Proc Natl Acad Sci U S A 106:20121–20126

    Article  PubMed Central  PubMed  Google Scholar 

  • Ross LO, Rankin S, Shuster MF, Dawson DS (1996) Effects of homology, size and exchange of the meiotic segregation of model chromosomes in Saccharomyces cerevisiae. Genetics 142:79–89

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sakuno T, Tanaka K, Hauf S, Watanabe Y (2011) Repositioning of aurora B promoted by chiasmata ensures sister chromatid mono-orientation in meiosis I. Dev Cell 21:534–545

    Article  PubMed  CAS  Google Scholar 

  • Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134:1109–1125

    Article  PubMed  CAS  Google Scholar 

  • Shonn MA, McCarroll R, Murray AW (2000) Requirement of the spindle checkpoint for proper chromosome segregation in budding yeast meiosis. Science 289:300–303

    Article  PubMed  CAS  Google Scholar 

  • Sourirajan A, Lichten M (2008) Polo-like kinase Cdc5 drives exit from pachytene during budding yeast meiosis. Genes Dev 22:2627–2632

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Speed RM (1977) The effects of ageing on the meiotic chromosomes of male and female mice. Chromosoma 64:241–254

    Article  PubMed  CAS  Google Scholar 

  • Stewart MN, Dawson DS (2004) Potential roles for centromere pairing in meiotic chromosome segregation. Cell Cycle 3:1232–1234

    Article  PubMed  CAS  Google Scholar 

  • Storlazzi A, Xu L, Schwacha A, Kleckner N (1996) Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc Natl Acad Sci U S A 93:9043–9048

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sturtevant AH, Beadle GW (1936) The relations of inversions in the X chromosome of Drosophila melanogaster to crossing over and disjunction. Genetics 21:554–604

    PubMed Central  PubMed  CAS  Google Scholar 

  • Sun F, Handel MA (2008) Regulation of the meiotic prophase I to metaphase I transition in mouse spermatocytes. Chromosoma 117:471–485

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Suzuki T, Ide N, Tanaka I (1997) Immunocytochemical visualization of the centromeres during male and female meiosis in Lilium longiflorum. Chromosoma 106:435–445

    Article  PubMed  CAS  Google Scholar 

  • Sym M, Roeder GS (1995) Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 128:455–466

    Article  PubMed  CAS  Google Scholar 

  • Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378

    Article  PubMed  CAS  Google Scholar 

  • Takeo S, Lake CM, Morais-de-Sa E, Sunkel CE, Hawley RS (2011) Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol: CB 21:1845–1851

    Article  PubMed  CAS  Google Scholar 

  • Tanneti NS, Landy K, Joyce EF, McKim KS (2011) A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol: CB 21:1852–1857

    Article  PubMed  CAS  Google Scholar 

  • Tarsounas M, Pearlman RE, Moens PB (1999) Meiotic activation of rat pachytene spermatocytes with okadaic acid: the behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3. J Cell Sci 112(Pt 4):423–434

    PubMed  CAS  Google Scholar 

  • Tease C, Hartshorne GM, Hulten MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70:1469–1479

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870–873

    Article  PubMed  CAS  Google Scholar 

  • Tsubouchi T, Macqueen AJ, Roeder GS (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22:3217–3226

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tung KS, Roeder GS (1998) Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149:817–832

    PubMed Central  PubMed  CAS  Google Scholar 

  • Vazquez J, Belmont AS, Sedat JW (2002) The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr Biol: CB 12:1473–1483

    Article  PubMed  CAS  Google Scholar 

  • Wang LH, Schwarzbraun T, Speicher MR, Nigg EA (2008) Persistence of DNA threads in human anaphase cells suggests late completion of sister chromatid decatenation. Chromosoma 117:123–135

    Google Scholar 

  • Wang K, Wang M, Tang D, Shen Y, Miao C, Hu Q, Lu T, Cheng Z (2012) The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet 8:e1002809

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Watanabe Y (2012) Geometry and force behind kinetochore orientation: lessons from meiosis. Nat Rev Mol Cell Biol 13:370–382

    Article  PubMed  CAS  Google Scholar 

  • Watts FZ, Hoffmann E (2011) SUMO meets meiosis: an encounter at the synaptonemal complex: SUMO chains and sumoylated proteins suggest that heterogeneous and complex interactions lie at the centre of the synaptonemal complex. BioEssays News Rev Mol Cell Dev Biol 33:529–537

    Article  CAS  Google Scholar 

  • Westermann S, Drubin DG, Barnes G (2007) Structures and functions of yeast kinetochore complexes. Annu Rev Biochem 76:563–591

    Article  PubMed  CAS  Google Scholar 

  • Wolf KW (1994) How meiotic cells deal with non-exchange chromosomes. BioEssays News Rev Mol Cell Dev Biol 16:107–114

    Article  CAS  Google Scholar 

  • Yu HG, Koshland D (2005) Chromosome morphogenesis: condensin-dependent cohesin removal during meiosis. Cell 123:397–407

    Article  PubMed  CAS  Google Scholar 

  • Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Ann Rev of Gen 32:619–697

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Scott Hawley and Emily Kurdzo for their comments on the manuscript. The authors acknowledge their colleagues in the Program of Cell Cycle and Cancer Biology for providing many thought-provoking discussions of centromere behavior in meiosis. RJP was supported by NIH NIGMS award 1P20GM103636 and by OCAST grant HR10-48S. DSD was supported by NIH NIGMS grant GM087377.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dean Dawson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Obeso, D., Pezza, R.J. & Dawson, D. Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma 123, 43–55 (2014). https://doi.org/10.1007/s00412-013-0439-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-013-0439-4

Keywords

Navigation