1932

Abstract

Production of gametes of halved ploidy for sexual reproduction requires a specialized cell division called meiosis. The fusion of two gametes restores the original ploidy in the new generation, and meiosis thus stabilizes ploidy across generations. To ensure balanced distribution of chromosomes, pairs of homologous chromosomes (homologs) must recognize each other and pair in the first meiotic division. Recombination plays a key role in this in most studied species, but it is not the only actor and particular chromosomal regions are known to facilitate the meiotic pairing of homologs. In this review, we focus on the roles of centromeres and in particular on the clustering and pairwise associations of nonhomologous centromeres that precede stable pairing between homologs. Although details vary from species to species, it is becoming increasingly clear that these associations play active roles in the meiotic chromosome pairing process, analogous to those of the telomere bouquet.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genet-112414-055107
2015-11-23
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/genet/49/1/annurev-genet-112414-055107.html?itemId=/content/journals/10.1146/annurev-genet-112414-055107&mimeType=html&fmt=ahah

Literature Cited

  1. Armstrong SJ, Franklin FC, Jones GH. 1.  2001. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114:4207–17 [Google Scholar]
  2. Bardhan A, Chuong H, Dawson DS. 2.  2010. Meiotic cohesin promotes pairing of nonhomologous centromeres in early meiotic prophase. Mol. Biol. Cell 21:1799–809 [Google Scholar]
  3. Barzel A, Kupiec M. 3.  2008. Finding a match: How do homologous sequences get together for recombination?. Nat. Rev. Genet. 9:27–37 [Google Scholar]
  4. Bass HW. 4.  2003. Telomere dynamics unique to meiotic prophase: formation and significance of the bouquet. Cell. Mol. Life Sci. 60:2319–24 [Google Scholar]
  5. Bass HW, Marshall WF, Sedat JW, Agard DA, Cande WZ. 5.  1997. 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. 137:5–18 [Google Scholar]
  6. Bass HW, Riera-Lizarazu O, Ananiev EV, Bordoli SJ, Rines HW. 6.  et al. 2000. Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J. Cell Sci. 113:Pt. 61033–42 [Google Scholar]
  7. Baudat F, Imai Y, de Massy B. 7.  2013. Meiotic recombination in mammals: localization and regulation. Nat. Rev. Genet. 14:794–806 [Google Scholar]
  8. Bhalla N, Dernburg AF. 8.  2008. Prelude to a division. Annu. Rev. Cell Dev. Biol. 24:397–424 [Google Scholar]
  9. Bisig CG, Guiraldelli MF, Kouznetsova A, Scherthan H, Hoog C. 9.  et al. 2012. Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLOS Genet. 8:e1002701 [Google Scholar]
  10. Black BE, Jansen LE, Foltz DR, Cleveland DW. 10.  2010. Centromere identity, function, and epigenetic propagation across cell divisions. Cold Spring Harb. Symp. Quant. Biol. 75:403–18 [Google Scholar]
  11. Bleuyard JY, White CI. 11.  2004. The Arabidopsis homologue of Xrcc3 plays an essential role in meiosis. EMBO J. 23:439–49 [Google Scholar]
  12. Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD. 12.  2013. Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev. Cell 24:196–205 [Google Scholar]
  13. Brown MS, Bishop DK. 13.  2015. DNA strand exchange and RecA homologs in meiosis. Cold Spring Harb. Perspect. Biol. 7:a016659 [Google Scholar]
  14. Burrack LS, Berman J. 14.  2012. Flexibility of centromere and kinetochore structures. Trends Genet. 28:204–12 [Google Scholar]
  15. Burrack LS, Berman J. 15.  2012. Neocentromeres and epigenetically inherited features of centromeres. Chromosome Res. 20:607–19 [Google Scholar]
  16. Cabral G, Marques A, Schubert V, Pedrosa-Harand A, Schlogelhofer P. 16.  2014. Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes. Nat. Commun. 5:5070 [Google Scholar]
  17. Cai X, Dong F, Edelmann RE, Makaroff CA. 17.  2003. The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J. Cell Sci. 116:2999–3007 [Google Scholar]
  18. Chen X. 18.  2012. Small RNAs in development: insights from plants. Curr. Opin. Genet. Dev. 22:361–67 [Google Scholar]
  19. Chikashige Y, Hiraoka Y. 19.  2001. Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr. Biol. 11:1618–23 [Google Scholar]
  20. Chikashige Y, Kinoshita N, Nakaseko Y, Matsumoto T, Murakami S. 20.  et al. 1989. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell 57:739–51 [Google Scholar]
  21. Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y. 21.  2006. Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125:59–69 [Google Scholar]
  22. Chowdhury D, Choi YE, Brault ME. 22.  2013. Charity begins at home: non-coding RNA functions in DNA repair. Nat. Rev. Mol. Cell Biol. 14:181–89 [Google Scholar]
  23. Church K, Moens PB. 23.  1976. Centromere behavior during interphase and meiotic prophase in Allium fistulosum from 3-D, EM reconstruction. Chromosoma 56:249–63 [Google Scholar]
  24. Clarke L, Carbon J. 24.  1980. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–9 [Google Scholar]
  25. Clarke L, Carbon J. 25.  1985. The structure and function of yeast centromeres. Annu. Rev. Genet. 19:29–55 [Google Scholar]
  26. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK. 26.  2012. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–25 [Google Scholar]
  27. Colas I, Shaw P, Prieto P, Wanous M, Spielmeyer W. 27.  et al. 2008. Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. PNAS 105:6075–80 [Google Scholar]
  28. Cooper JP, Watanabe Y, Nurse P. 28.  1998. Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392:828–31 [Google Scholar]
  29. Corredor E, Lukaszewski AJ, Pachon P, Allen DC, Naranjo T. 29.  2007. Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177:699–706 [Google Scholar]
  30. Cowan CR, Cande WZ. 30.  2002. Meiotic telomere clustering is inhibited by colchicine but does not require cytoplasmic microtubules. J. Cell Sci. 115:3747–56 [Google Scholar]
  31. Cowan CR, Carlton PM, Cande WZ. 31.  2002. Reorganization and polarization of the meiotic bouquet-stage cell can be uncoupled from telomere clustering. J. Cell Sci. 115:3757–66 [Google Scholar]
  32. Da Ines O, Abe K, Goubely C, Gallego ME, White CI. 32.  2012. Differing requirements for RAD51 and DMC1 in meiotic pairing of centromeres and chromosome arms in Arabidopsis thaliana. PLOS Genet. 8:e1002636 [Google Scholar]
  33. Da Ines O, Degroote F, Goubely C, Amiard S, Gallego ME, White CI. 33.  2013. Meiotic recombination in Arabidopsis is catalysed by DMC1, with RAD51 playing a supporting role. PLOS Genet. 9:e1003787 [Google Scholar]
  34. Da Ines O, Gallego ME, White CI. 34.  2014. Recombination-independent mechanisms and pairing of homologous chromosomes during meiosis in plants. Mol. Plant 7:492–501 [Google Scholar]
  35. de Massy B. 35.  2013. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47:563–99 [Google Scholar]
  36. De Rop V, Padeganeh A, Maddox PS. 36.  2012. CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 121:527–38 [Google Scholar]
  37. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. 37.  1998. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–98 [Google Scholar]
  38. Dernburg AF, Sedat JW, Hawley RS. 38.  1996. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135–46 [Google Scholar]
  39. Ding DQ, Haraguchi T, Hiraoka Y. 39.  2012. Chromosomally-retained RNA mediates homologous pairing. Nucleus 3:516–19 [Google Scholar]
  40. Ding DQ, Haraguchi T, Hiraoka Y. 40.  2013. The role of chromosomal retention of noncoding RNA in meiosis. Chromosome Res. 21:665–72 [Google Scholar]
  41. Ding DQ, Okamasa K, Yamane M, Tsutsumi C, Haraguchi T. 41.  et al. 2012. Meiosis-specific noncoding RNA mediates robust pairing of homologous chromosomes in meiosis. Science 336:732–36 [Google Scholar]
  42. Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y. 42.  2004. Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev. Cell 6:329–41 [Google Scholar]
  43. Falk JE, Chan AC, Hoffmann E, Hochwagen A. 43.  2010. A Mec1- and PP4-dependent checkpoint couples centromere pairing to meiotic recombination. Dev. Cell 19:599–611 [Google Scholar]
  44. Fennell A, Fernandez-Alvarez A, Tomita K, Cooper JP. 44.  2015. Telomeres and centromeres have interchangeable roles in promoting meiotic spindle formation. J. Cell Biol. 208:415–28 [Google Scholar]
  45. Flemming W. 45.  1882. Zellsubstanz, Kern und Zelltheilung Leipzig: F.C.W. Vogel [Google Scholar]
  46. Fransz P, Armstrong S, Alonso-Blanco C, Fischer TC, Torres-Ruiz RA, Jones G. 46.  1998. Cytogenetics for the model system Arabidopsis thaliana. Plant J. 13:867–76 [Google Scholar]
  47. Fukagawa T, Earnshaw WC. 47.  2014. The centromere: chromatin foundation for the kinetochore machinery. Dev. Cell 30:496–508 [Google Scholar]
  48. Gerton JL, Hawley RS. 48.  2005. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat. Rev. Genet. 6:477–87 [Google Scholar]
  49. Gladstone MN, Obeso D, Chuong H, Dawson DS. 49.  2009. The synaptonemal complex protein Zip1 promotes bi-orientation of centromeres at meiosis I. PLOS Genet. 5:e1000771 [Google Scholar]
  50. Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ. 50.  2002. The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162:1979–93 [Google Scholar]
  51. Greer E, Martin AC, Pendle A, Colas I, Jones AM. 51.  et al. 2012. The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24:152–62 [Google Scholar]
  52. Guerra M, Cabral G, Cuacos M, Gonzalez-Garcia M, Gonzalez-Sanchez M. 52.  et al. 2010. Neocentrics and holokinetics (holocentrics): chromosomes out of the centromeric rules. Cytogenet. Genome Res. 129:82–96 [Google Scholar]
  53. Harper L, Golubovskaya I, Cande WZ. 53.  2004. A bouquet of chromosomes. J. Cell Sci. 117:4025–32 [Google Scholar]
  54. Hawley RS, Theurkauf WE. 54.  1993. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 9:310–17 [Google Scholar]
  55. Heckmann S, Jankowska M, Schubert V, Kumke K, Ma W, Houben A. 55.  2014. Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans. Nat. Commun. 5:4979 [Google Scholar]
  56. Heckmann S, Schubert V, Houben A. 56.  2014. Holocentric plant meiosis: first sisters, then homologues. Cell Cycle 13:3623–24 [Google Scholar]
  57. Henderson KA, Keeney S. 57.  2005. Synaptonemal complex formation: Where does it start?. BioEssays 27:995–98 [Google Scholar]
  58. Henikoff S, Furuyama T. 58.  2010. Epigenetic inheritance of centromeres. Cold Spring Harb. Symp. Quant. Biol. 75:51–60 [Google Scholar]
  59. Higgins JD, Osman K, Jones GH, Franklin FC. 59.  2014. Factors underlying restricted crossover localization in barley meiosis. Annu. Rev. Genet. 48:29–47 [Google Scholar]
  60. Higgins JD, Perry RM, Barakate A, Ramsay L, Waugh R. 60.  et al. 2012. Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24:4096–109 [Google Scholar]
  61. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC. 61.  2005. The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev. 19:2488–500 [Google Scholar]
  62. Hotta Y, Tabata S, Stubbs L, Stern H. 62.  1985. Meiosis-specific transcripts of a DNA component replicated during chromosome pairing: homology across the phylogenetic spectrum. Cell 40:785–93 [Google Scholar]
  63. Houben A, Schubert I. 63.  2003. DNA and proteins of plant centromeres. Curr. Opin. Plant Biol. 6:554–60 [Google Scholar]
  64. Jiang J, Birchler JA, Parrott WA, Dawe RK. 64.  2003. A molecular view of plant centromeres. Trends Plant Sci. 8:570–75 [Google Scholar]
  65. Karpen GH, Le MH, Le H. 65.  1996. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273:118–22 [Google Scholar]
  66. Kemp B, Boumil RM, Stewart MN, Dawson DS. 66.  2004. A role for centromere pairing in meiotic chromosome segregation. Genes Dev. 18:1946–51 [Google Scholar]
  67. Klutstein M, Cooper JP. 67.  2014. The chromosomal courtship dance: homolog pairing in early meiosis. Curr. Opin. Cell Biol. 26:123–31 [Google Scholar]
  68. Klutstein M, Fennell A, Fernandez-Alvarez A, Cooper JP. 68.  2015. The telomere bouquet regulates meiotic centromere assembly. Nat. Cell Biol. 17:458–69 [Google Scholar]
  69. Lam I, Keeney S. 69.  2015. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7:a016634 [Google Scholar]
  70. Lamb JC, Yu W, Han F, Birchler JA. 70.  2007. Plant chromosomes from end to end: telomeres, heterochromatin and centromeres. Curr. Opin. Plant Biol. 10:116–22 [Google Scholar]
  71. Lee CY, Conrad MN, Dresser ME. 71.  2012. Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLOS Genet. 8:e1002730 [Google Scholar]
  72. Leu JY, Chua PR, Roeder GS. 72.  1998. The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell 94:375–86 [Google Scholar]
  73. Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E. 73.  et al. 2004. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. PNAS 101:10596–601 [Google Scholar]
  74. Li W, Yang X, Lin Z, Timofejeva L, Xiao R. 74.  et al. 2005. The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol. 138:965–76 [Google Scholar]
  75. Liu L, Franco S, Spyropoulos B, Moens PB, Blasco MA, Keefe DL. 75.  2004. Irregular telomeres impair meiotic synapsis and recombination in mice. PNAS 101:6496–501 [Google Scholar]
  76. Loidl J. 76.  1990. The initiation of meiotic chromosome pairing: the cytological view. Genome 33:759–78 [Google Scholar]
  77. Loidl J, Lukaszewicz A, Howard-Till RA, Koestler T. 77.  2012. The Tetrahymena meiotic chromosome bouquet is organized by centromeres and promotes interhomolog recombination. J. Cell Sci. 125:5873–80 [Google Scholar]
  78. Ma J, Wing RA, Bennetzen JL, Jackson SA. 78.  2007. Plant centromere organization: a dynamic structure with conserved functions. Trends Genet. 23:134–39 [Google Scholar]
  79. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. 79.  2005. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037–50 [Google Scholar]
  80. Martinez-Perez E, Schvarzstein M, Barroso C, Lightfoot J, Dernburg AF, Villeneuve AM. 80.  2008. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22:2886–901 [Google Scholar]
  81. Martinez-Perez E, Shaw P, Aragon-Alcaide L, Moore G. 81.  2003. Chromosomes form into seven groups in hexaploid and tetraploid wheat as a prelude to meiosis. Plant J. 36:21–29 [Google Scholar]
  82. Martinez-Perez E, Shaw P, Moore G. 82.  2001. The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411:204–7 [Google Scholar]
  83. Martinez-Perez E, Shaw P, Reader S, Aragon-Alcaide L, Miller T, Moore G. 83.  1999. Homologous chromosome pairing in wheat. J. Cell Sci. 112:Pt. 111761–69 [Google Scholar]
  84. Martinez-Perez E, Shaw PJ, Moore G. 84.  2000. Polyploidy induces centromere association. J. Cell Biol. 148:233–38 [Google Scholar]
  85. McKee BD. 85.  1996. The license to pair: identification of meiotic pairing sites in Drosophila. Chromosoma 105:135–41 [Google Scholar]
  86. McKee BD. 86.  2009. Homolog pairing and segregation in Drosophila meiosis. Genome Dyn. 5:56–68 [Google Scholar]
  87. McKee BD, Habera L, Vrana JA. 87.  1992. Evidence that intergenic spacer repeats of Drosophila melanogaster rRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing. Genetics 132:529–44 [Google Scholar]
  88. McKee BD, Karpen GH. 88.  1990. Drosophila ribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell 61:61–72 [Google Scholar]
  89. McKee BD, Yan R, Tsai JH. 89.  2012. Meiosis in male Drosophila. Spermatogenesis 2:167–84 [Google Scholar]
  90. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C. 90.  et al. 1998. Meiotic synapsis in the absence of recombination. Science 279:876–78 [Google Scholar]
  91. Melters DP, Paliulis LV, Korf IF, Chan SW. 91.  2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 20:579–93 [Google Scholar]
  92. Mercier R, Mezard C, Jenczewski E, Macaisne N, Grelon M. 92.  2014. The molecular biology of meiosis in plants. Annu. Rev. Plant Biol. 66:297–327 [Google Scholar]
  93. Moore G, Shaw P. 93.  2009. Improving the chances of finding the right partner. Curr. Opin. Genet. Dev. 19:99–104 [Google Scholar]
  94. Nag DK, Scherthan H, Rockmill B, Bhargava J, Roeder GS. 94.  1995. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141:75–86 [Google Scholar]
  95. Nagaki K, Walling J, Hirsch C, Jiang J, Murata M. 95.  2009. Structure and evolution of plant centromeres. Prog. Mol. Subcell. Biol. 48:153–79 [Google Scholar]
  96. Nagaoka SI, Hassold TJ, Hunt PA. 96.  2012. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat. Rev. Genet. 13:493–504 [Google Scholar]
  97. Naranjo T, Corredor E. 97.  2008. Nuclear architecture and chromosome dynamics in the search of the pairing partner in meiosis in plants. Cytogenet. Genome Res. 120:320–30 [Google Scholar]
  98. Newnham L, Jordan P, Rockmill B, Roeder GS, Hoffmann E. 98.  2010. The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I. PNAS 107:781–85 [Google Scholar]
  99. Obeso D, Dawson DS. 99.  2010. Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLOS ONE 5:e10336 [Google Scholar]
  100. Obeso D, Pezza RJ, Dawson D. 100.  2014. Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma 123:43–55 [Google Scholar]
  101. Pecinka A, Schubert V, Meister A, Kreth G, Klatte M. 101.  et al. 2004. Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113:258–69 [Google Scholar]
  102. Phillips CM, Dernburg AF. 102.  2006. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11:817–29 [Google Scholar]
  103. Phillips CM, Meng X, Zhang L, Chretien JH, Urnov FD, Dernburg AF. 103.  2009. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat. Cell Biol. 11:934–42 [Google Scholar]
  104. Phillips D, Nibau C, Wnetrzak J, Jenkins G. 104.  2012. High resolution analysis of meiotic chromosome structure and behaviour in barley (Hordeum vulgare L.). PLOS ONE 7:e39539 [Google Scholar]
  105. Prieto P, Moore G, Reader S. 105.  2005. Control of conformation changes associated with homologue recognition during meiosis. Theor. Appl. Genet. 111:505–10 [Google Scholar]
  106. Prieto P, Santos AP, Moore G, Shaw P. 106.  2004. Chromosomes associate premeiotically and in xylem vessel cells via their telomeres and centromeres in diploid rice (Oryza sativa). Chromosoma 112:300–7 [Google Scholar]
  107. Prieto P, Shaw P, Moore G. 107.  2004. Homologue recognition during meiosis is associated with a change in chromatin conformation. Nat. Cell Biol. 6:906–8 [Google Scholar]
  108. Qiao H, Chen JK, Reynolds A, Hoog C, Paddy M, Hunter N. 108.  2012. Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLOS Genet. 8:e1002790 [Google Scholar]
  109. Roberts NY, Osman K, Armstrong SJ. 109.  2009. Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet. Genome Res. 124:193–201 [Google Scholar]
  110. Roberts NY, Osman K, Franklin FC, Pradillo M, Varas J. 110.  et al. 2013. Telomeres in plant meiosis: their structure, dynamics and function. Annu. Plant Rev. 46:191–228 [Google Scholar]
  111. Rockmill B, Sym M, Scherthan H, Roeder GS. 111.  1995. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9:2684–95 [Google Scholar]
  112. Rog O, Dernburg AF. 112.  2013. Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr. Opin. Cell Biol. 25:349–56 [Google Scholar]
  113. Ronceret A, Doutriaux MP, Golubovskaya IN, Pawlowski WP. 113.  2009. PHS1 regulates meiotic recombination and homologous chromosome pairing by controlling the transport of RAD50 to the nucleus. PNAS 106:20121–26 [Google Scholar]
  114. Ross KJ, Fransz P, Jones GH. 114.  1996. A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 4:507–16 [Google Scholar]
  115. Scherthan H. 115.  2001. A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2:621–27 [Google Scholar]
  116. Scherthan H, Weich S, Schwegler H, Heyting C, Harle M, Cremer T. 116.  1996. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134:1109–25 [Google Scholar]
  117. Scott KC, Sullivan BA. 117.  2014. Neocentromeres: a place for everything and everything in its place. Trends Genet. 30:66–74 [Google Scholar]
  118. Sonntag Brown M, Zanders S, Alani E. 118.  2011. Sustained and rapid chromosome movements are critical for chromosome pairing and meiotic progression in budding yeast. Genetics 188:21–32 [Google Scholar]
  119. Stewart MN, Dawson DS. 119.  2008. Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet. 24:564–73 [Google Scholar]
  120. Stronghill P, Pathan N, Ha H, Supijono E, Hasenkampf C. 120.  2010. Ahp2 (Hop2) function in Arabidopsis thaliana (Ler) is required for stabilization of close alignment and synaptonemal complex formation except for the two short arms that contain nucleolus organizer regions. Chromosoma 119:443–58 [Google Scholar]
  121. Sun X, Le HD, Wahlstrom JM, Karpen GH. 121.  2003. Sequence analysis of a functional Drosophila centromere. Genome Res. 13:182–94 [Google Scholar]
  122. Takeo S, Lake CM, Morais-de-Sa E, Sunkel CE, Hawley RS. 122.  2011. Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr. Biol. 21:1845–51 [Google Scholar]
  123. Tanneti NS, Landy K, Joyce EF, McKim KS. 123.  2011. A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr. Biol. 21:1852–57 [Google Scholar]
  124. Tomita K, Cooper JP. 124.  2006. The meiotic chromosomal bouquet: SUN collects flowers. Cell 125:19–21 [Google Scholar]
  125. Tomita K, Cooper JP. 125.  2007. The telomere bouquet controls the meiotic spindle. Cell 130:113–26 [Google Scholar]
  126. Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H. 126.  2005. Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol. 170:213–23 [Google Scholar]
  127. Trelles-Sticken E, Dresser ME, Scherthan H. 127.  2000. Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151:95–106 [Google Scholar]
  128. Trelles-Sticken E, Loidl J, Scherthan H. 128.  1999. Bouquet formation in budding yeast: initiation of recombination is not required for meiotic telomere clustering. J. Cell Sci. 112:Pt. 5651–58 [Google Scholar]
  129. Tsai JH, McKee BD. 129.  2011. Homologous pairing and the role of pairing centers in meiosis. J. Cell Sci. 124:1955–63 [Google Scholar]
  130. Tsubouchi H, Roeder GS. 130.  2003. The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell 5:915–25 [Google Scholar]
  131. Tsubouchi T, Macqueen AJ, Roeder GS. 131.  2008. Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev. 22:3217–26 [Google Scholar]
  132. Tsubouchi T, Roeder GS. 132.  2005. A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870–73 [Google Scholar]
  133. Wang G, Zhang X, Jin W. 133.  2009. An overview of plant centromeres. J. Genet. Genomics 36:529–37 [Google Scholar]
  134. Weiner BM, Kleckner N. 134.  1994. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977–91 [Google Scholar]
  135. Wen R, Moore G, Shaw PJ. 135.  2012. Centromeres cluster de novo at the beginning of meiosis in Brachypodium distachyon. PLOS ONE 7:e44681 [Google Scholar]
  136. Willard HF. 136.  1990. Centromeres of mammalian chromosomes. Trends Genet. 6:410–16 [Google Scholar]
  137. Wilson PJ, Riggs CD, Hasenkampf CA. 137.  2005. Plant chromosome homology: hypotheses relating rendezvous, recognition and reciprocal exchange. Cytogenet. Genome Res. 109:190–97 [Google Scholar]
  138. Xiang Y, Miller DE, Ross EJ, Sanchez Alvarado A, Hawley RS. 138.  2014. Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea. PNAS 111:E5159–68 [Google Scholar]
  139. Xu M, Cook PR. 139.  2008. The role of specialized transcription factories in chromosome pairing. Biochim. Biophys. Acta 1783:2155–60 [Google Scholar]
  140. Yamagishi Y, Sakuno T, Goto Y, Watanabe Y. 140.  2014. Kinetochore composition and its function: lessons from yeasts. FEMS Microbiol. Rev. 38:185–200 [Google Scholar]
  141. Yang H, Lu P, Wang Y, Ma H. 141.  2011. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. 65:503–16 [Google Scholar]
  142. Yang X, Boateng KA, Strittmatter L, Burgess R, Makaroff CA. 142.  2009. Arabidopsis separase functions beyond the removal of sister chromatid cohesion during meiosis. Plant Physiol. 151:323–33 [Google Scholar]
  143. Yang X, Timofejeva L, Ma H, Makaroff CA. 143.  2006. The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J. Cell Sci. 119:3754–63 [Google Scholar]
  144. Zetka M. 144.  2009. Homologue pairing, recombination and segregation in Caenorhabditis elegans. Genome Dyn. 5:43–55 [Google Scholar]
  145. Zhang J, Pawlowski WP, Han F. 145.  2013. Centromere pairing in early meiotic prophase requires active centromeres and precedes installation of the synaptonemal complex in maize. Plant Cell 25:3900–9 [Google Scholar]
  146. Zickler D. 146.  2006. From early homologue recognition to synaptonemal complex formation. Chromosoma 115:158–74 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-055107
Loading
/content/journals/10.1146/annurev-genet-112414-055107
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error