, 120:447 | Cite as

The template choice decision in meiosis: is the sister important?



Recombination between homologous chromosomes is crucial to ensure their proper segregation during meiosis. This is achieved by regulating the choice of recombination template. In mitotic cells, double-strand break repair with the sister chromatid appears to be preferred, whereas interhomolog recombination is favoured during meiosis. However, in the last year, several studies in yeast have shown the importance of the meiotic recombination between sister chromatids. Although this thinking seems to be new, evidences for sister chromatid exchange during meiosis were obtained more than 50 years ago in non-model organisms. In this mini-review, we comment briefly on the most recent advances in this hot topic and also describe observations which suggest the existence of inter-sister repair during meiotic recombination. For instance, the behaviour of mammalian XY bivalents and that of trivalents in heterozygotes for chromosomal rearrangements are cited as examples. The “rediscovering” of the requirement for the sister template, although it seems to occur at a low frequency, will probably prompt further investigations in organisms other than yeast to understand the complexity of the partner choice during meiosis.

List of abbreviations


Axial element




Barrier to sister chromatid repair




Double Holliday junction


Double-strand break


DSB repair


Fluorescent plus Giemsa


Interhomolog recombination




Synaptonemal complex


Sister chromatid exchange


Synthesis-dependent strand annealing


Single-end invasion


Single-strand DNA


  1. Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57PubMedCrossRefGoogle Scholar
  2. Andersen SL, Sekelsky J (2010) Meiotic versus mitotic recombination: two different routes for double-strand break repair: the different functions of meiotic versus mitotic DSB repair are reflected in different pathway usage and different outcomes. Bioessays 32:1058–1066PubMedCrossRefGoogle Scholar
  3. Ashley T, Plug AW, Xu J, Solari AJ, Reddy G, Golub EI, Ward DC (1995) Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates. Chromosoma 104:19–28PubMedCrossRefGoogle Scholar
  4. Barlow AL, Benson FE, West SC, Hultén MA (1997) Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J 16:5207–5215PubMedCrossRefGoogle Scholar
  5. Bishop DK, Park D, Xu LZ, Kleckner N (1992) DMC1: a meiosis-specific yeast homolog of Escherichia coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439–456PubMedCrossRefGoogle Scholar
  6. Brewen JG, Peacock WJ (1969) The effect of tritiated thymidine on sister-chromatid exchange in a ring chromosome. Mutat Res 7:433–440PubMedGoogle Scholar
  7. Callender T, Hollingsworth NM (2010) Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics 185:771–782PubMedCrossRefGoogle Scholar
  8. Calvente A, Viera A, Page J, Parra MT, Gómez R, Suja JA, Rufas JS, Santos JL (2005) DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis. J Cell Sci 118:2957–2963PubMedCrossRefGoogle Scholar
  9. Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089–1101PubMedCrossRefGoogle Scholar
  10. Carballo JA, Johnson AL, Sedgwick SG, Cha RS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132:758–770PubMedCrossRefGoogle Scholar
  11. Chicheportiche A, Bernardino-Sgherri J, de Massy B, Dutrillaux B (2007) Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse. J Cell Sci 120:1733–1742PubMedCrossRefGoogle Scholar
  12. Church K, Wimber DE (1969) Meiosis in the grasshopper: chiasma frequency after elevated temperature and x-rays. Can J Genet Cytol 11:209–216PubMedGoogle Scholar
  13. Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19:2744–2756PubMedCrossRefGoogle Scholar
  14. Couteau F, Zetka M (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20:353–363PubMedCrossRefGoogle Scholar
  15. Couteau F, Nabeshima K, Villeneuve A, Zetka M (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol 14:585–592PubMedCrossRefGoogle Scholar
  16. Craig-Cameron T, Jones GH (1970) The analysis of exchanges in tritium-labelled meiotic chromosomes. 1. Heredity 25:223–232PubMedCrossRefGoogle Scholar
  17. de Jong JH, Havekes F, Roca A, Naranjo T (1991) Synapsis and chiasma formation in a ditelo-substituted haploid of rye. Genome 34:109–120CrossRefGoogle Scholar
  18. de la Fuente R, Parra MT, Viera A, Calvente A, Gómez 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:e198PubMedCrossRefGoogle Scholar
  19. Goldfarb T, Lichten M (2010) Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLoS Biol 8:e1000520PubMedCrossRefGoogle Scholar
  20. Green MM (1968) Some genetic properties of intrachromosomal recombination. Mol Gen Genet 103:209–217PubMedCrossRefGoogle Scholar
  21. Hochwagen A, Amon A (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16:R217–R228PubMedCrossRefGoogle Scholar
  22. Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106:59–70PubMedCrossRefGoogle Scholar
  23. Hyppa RW, Smith GR (2010) Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 142:243–255PubMedCrossRefGoogle Scholar
  24. Jessop L, Allers T, Lichten M (2005) Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169:1353–1367PubMedCrossRefGoogle Scholar
  25. Jones GH (1971) The analysis of exchanges in tritium-labelled meiotic chromosomes. II. Stethophyma grossum. Chromosoma 34:367–382CrossRefGoogle Scholar
  26. Jones GH, Brumpton RJ (1971) Sister and non-sister chromatid U-type exchange in rye meiosis. Chromosoma 33:115–128CrossRefGoogle Scholar
  27. Kato H (1977) Spontaneous and induced sister chromatid exchanges as revealed by the BUdR-labeling method. Int Rev Cytol 49:55–97PubMedCrossRefGoogle Scholar
  28. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1–53PubMedCrossRefGoogle Scholar
  29. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, Kleckner N (2010) Sister cohesion and meiotic axis components mediate homolog bias of meiotic recombination. Cell 143:924–937PubMedCrossRefGoogle Scholar
  30. Latypov V, Rothenberg M, Lorenz A, Octobre G, Csutak O, Lehmann E, Loidl J, Kohli J (2010) Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Mol Cell Biol 30:1570–1581PubMedCrossRefGoogle Scholar
  31. Loidl J, Nairz K (1997) Karyotype variability in yeast caused by nonallelic recombination in haploid meiosis. Genetics 146:79–88PubMedGoogle Scholar
  32. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodríguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271–276PubMedCrossRefGoogle Scholar
  33. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–485PubMedCrossRefGoogle Scholar
  34. Manterola M, Page J, Vasco C, Berríos S, Parra MT, Viera A, Rufas JS, Zuccotti M, Garagna S, Fernández-Donoso R (2009) A high incidence of meiotic silencing of unsynapsed chromatin is not associated with substantial pachytene loss in heterozygous male mice carrying multiple simple robertsonian translocations. PLoS Genet 5:e1000625PubMedCrossRefGoogle Scholar
  35. Martinez-Perez E, Villeneuve AM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19:2727–2743PubMedCrossRefGoogle Scholar
  36. Mazrimas JA, Stetka DG (1978) Direct evidence for the role of incorporated BUdR in the induction of sister chromatid exchanges. Exp Cell Res 117:23–30PubMedCrossRefGoogle Scholar
  37. McMahill MS, Sham CW, Bishop DK (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5:e299PubMedCrossRefGoogle Scholar
  38. Merker JD, Dominska M, Petes TD (2003) Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165:47–63PubMedGoogle Scholar
  39. Michaelis A (1959) Behavior of the ring chromosomes in mitosis and meiosis in Antirrhinum majus L. Chromosoma 10:144–162PubMedCrossRefGoogle Scholar
  40. Moens PB, Chen DJ, Shen Z, Kolas N, Tarsounas M, Heng HH, Spyropoulos B (1997) Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106:207–215PubMedCrossRefGoogle Scholar
  41. Nag DK, Petes TD (1993) Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol 13:2324–2331PubMedGoogle Scholar
  42. Neijzing MG (1982) Chiasma formation in duplicated segments of the haploid rye genome. Chromosoma 85:287–298CrossRefGoogle Scholar
  43. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, Hollingsworth NM (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16:5804–5818PubMedCrossRefGoogle Scholar
  44. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, Kunz RC, Kubota K, Wang B, Sung P, Shokat KM, Gygi SP, Hollingsworth NM (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 36:393–404PubMedCrossRefGoogle Scholar
  45. Page J, de la Fuente R, Gómez R, Calvente A, Viera A, Parra MT, Santos JL, Berríos S, Fernández-Donoso R, Suja JA, Rufas JS (2006) Sex chromosomes, synapsis, and cohesins: a complex affair. Chromosoma 115:250–259PubMedCrossRefGoogle Scholar
  46. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, Zhu X, Neale MJ, Jasin M, Socci ND, Hochwagen A, Keeney S (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144:719–731PubMedCrossRefGoogle Scholar
  47. Peacock WJ (1968) Replication, recombination and chiasmata in Goniaea australasie (Orthoptera, Acrididae). Genetics 65:593–617Google Scholar
  48. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868PubMedCrossRefGoogle Scholar
  49. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM (2000) Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275:9390–9395PubMedCrossRefGoogle Scholar
  50. Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220–2233PubMedCrossRefGoogle Scholar
  51. Santos JL, Jiménez MM, Díez M (1994) Meiosis in haploid rye: extensive synapsis and low chiasma frequency. Heredity 73:580–588CrossRefGoogle Scholar
  52. Schwartz D (1953) Evidence for sister-strand crossing over in maize. Genetics 38:251–260PubMedGoogle Scholar
  53. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, Wang PJ, Meistrich ML, Rajkovic A (2010) Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet 6:e1001190PubMedCrossRefGoogle Scholar
  54. Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470PubMedCrossRefGoogle Scholar
  55. Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136:957–967PubMedCrossRefGoogle Scholar
  56. Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437–451PubMedCrossRefGoogle Scholar
  57. Suja JA, del Cerro AL, Page J, Rufas JS, Santos JL (2000) Meiotic sister chromatid cohesion in holocentric sex chromosomes of three heteropteran species is maintained in absence of axial elements. Chromosoma 109:35–43PubMedCrossRefGoogle Scholar
  58. Sun H, Treco D, Schultes NP, Szostak JW (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338:87–90PubMedCrossRefGoogle Scholar
  59. Sun H, Treco D, Szostak JW (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64:1155–1161PubMedCrossRefGoogle Scholar
  60. Taylor JH (1965) Distribution of tritium-labeled DNA among chromosomes during meiosis: I. Spermatogenesis in the grasshopper. J Cell Biol 25:57–68PubMedCrossRefGoogle Scholar
  61. Tease C (1978) Cytological detection of crossing-over in BUdR substituted meiotic chromosomes using the fluorescent plus Giemsa technique. Nature 272:823–824PubMedCrossRefGoogle Scholar
  62. Tease C, Jones GH (1979) Analysis of exchanges in differentially stained meiotic chromosomes of Locusta migratoria after BrdU-substitution and FPG staining. Chromosoma 73:75–84CrossRefGoogle Scholar
  63. Tease C, Jones GH (1995) Do chiasmata disappear? An examination of whether closely spaced chiasmata are liable to reduction or loss. Chromosome Res 3:162–168PubMedCrossRefGoogle Scholar
  64. Terentyev Y, Johnson R, Neale MJ, Khisroon M, Bishop-Bailey A, Goldman AS (2010) Evidence that MEK1 positively promotes interhomologue double-strand break repair. Nucleic Acids Res 38:4349–4360PubMedCrossRefGoogle Scholar
  65. Tsubouchi H, Roeder GS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20:1766–1775PubMedCrossRefGoogle Scholar
  66. Viera A, Santos JL, Page J, Parra MT, Calvente A, Cifuentes M, Gómez R, Lira R, Suja JA, Rufas JS (2004a) DNA double-strand breaks, recombination and synapsis: the timing of meiosis differs in grasshoppers and flies. EMBO Rep 5:385–391PubMedCrossRefGoogle Scholar
  67. Viera A, Calvente A, Page J, Parra MT, Gómez R, Suja JA, Rufas JS, Santos JL (2004b) X and B chromosomes display similar meiotic characteristics in male grasshoppers. Cytogenet Genome Res 106:302–308PubMedCrossRefGoogle Scholar
  68. Viera A, Santos JL, Rufas JS (2009a) Relationship between incomplete synapsis and chiasma localization. Chromosoma 118:377–389PubMedCrossRefGoogle Scholar
  69. Viera A, Santos JL, Parra MT, Calvente A, Gómez R, de la Fuente R, Suja JA, Page J, Rufas JS (2009b) Cohesin axis maturation and presence of RAD51 during first meiotic prophase in a true bug. Chromosoma 118:575–589PubMedCrossRefGoogle Scholar
  70. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, McKay MJ, Toth A (2010) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5:e1000702CrossRefGoogle Scholar
  71. Wolff S (1979) Sister chromatid exchange. Ann Rev Genet 11:183–201CrossRefGoogle Scholar
  72. Wolff S, Perry P (1974) Differential Giemsa staining of sister chromatids and the study of sister chromatid exchanges without autoradiography. Chromosoma 48:341–353PubMedCrossRefGoogle Scholar
  73. Zanders S, Sonntag Brown M, Chen C, Alani E (2011) Pch2 modulates chromatid partner choice during meiotic double-strand break repair in Saccharomyces cerevisiae. Genetics 188:511–521Google Scholar
  74. Zetka MC, Kawasaki I, Strome S, Müller F (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev 13:2258–2270PubMedCrossRefGoogle Scholar
  75. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Departamento de Genética, Facultad de BiologíaUniversidad Complutense de MadridMadridSpain

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