Skip to main content
Log in

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

  • Mini-Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

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.

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

Similar content being viewed by others

Abbreviations

AE:

Axial element

BrdU:

Bromodeoxyuridine

BSCR:

Barrier to sister chromatid repair

CO:

Crossover

dHJ:

Double Holliday junction

DSB:

Double-strand break

DSBR:

DSB repair

FPG:

Fluorescent plus Giemsa

IHR:

Interhomolog recombination

NCO:

Non-crossover

SC:

Synaptonemal complex

SCE:

Sister chromatid exchange

SDSA:

Synthesis-dependent strand annealing

SEI:

Single-end invasion

ssDNA:

Single-strand DNA

References

  • Allers T, Lichten M (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106:47–57

    Article  PubMed  CAS  Google Scholar 

  • 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 32:1058–1066

    Article  PubMed  CAS  Google Scholar 

  • 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 104:19–28

    Article  PubMed  CAS  Google Scholar 

  • Barlow AL, Benson FE, West SC, Hultén MA (1997) Distribution of the Rad51 recombinase in human and mouse spermatocytes. EMBO J 16:5207–5215

    Article  PubMed  CAS  Google Scholar 

  • 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 69:439–456

    Article  PubMed  CAS  Google Scholar 

  • Brewen JG, Peacock WJ (1969) The effect of tritiated thymidine on sister-chromatid exchange in a ring chromosome. Mutat Res 7:433–440

    PubMed  CAS  Google Scholar 

  • 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 185:771–782

    Article  PubMed  CAS  Google Scholar 

  • 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 118:2957–2963

    Article  PubMed  CAS  Google Scholar 

  • Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61:1089–1101

    Article  PubMed  CAS  Google Scholar 

  • Carballo JA, Johnson AL, Sedgwick SG, Cha RS (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132:758–770

    Article  PubMed  CAS  Google Scholar 

  • 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 120:1733–1742

    Article  PubMed  CAS  Google Scholar 

  • Church K, Wimber DE (1969) Meiosis in the grasshopper: chiasma frequency after elevated temperature and x-rays. Can J Genet Cytol 11:209–216

    PubMed  CAS  Google Scholar 

  • Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19:2744–2756

    Article  PubMed  CAS  Google Scholar 

  • Couteau F, Zetka M (2011) DNA damage during meiosis induces chromatin remodeling and synaptonemal complex disassembly. Dev Cell 20:353–363

    Article  PubMed  CAS  Google Scholar 

  • 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 14:585–592

    Article  PubMed  CAS  Google Scholar 

  • Craig-Cameron T, Jones GH (1970) The analysis of exchanges in tritium-labelled meiotic chromosomes. 1. Heredity 25:223–232

    Article  PubMed  CAS  Google Scholar 

  • de Jong JH, Havekes F, Roca A, Naranjo T (1991) Synapsis and chiasma formation in a ditelo-substituted haploid of rye. Genome 34:109–120

    Article  Google Scholar 

  • 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:e198

    Article  PubMed  Google Scholar 

  • 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:e1000520

    Article  PubMed  Google Scholar 

  • Green MM (1968) Some genetic properties of intrachromosomal recombination. Mol Gen Genet 103:209–217

    Article  PubMed  CAS  Google Scholar 

  • Hochwagen A, Amon A (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16:R217–R228

    Article  PubMed  CAS  Google Scholar 

  • 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 106:59–70

    Article  PubMed  CAS  Google Scholar 

  • Hyppa RW, Smith GR (2010) Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 142:243–255

    Article  PubMed  CAS  Google Scholar 

  • Jessop L, Allers T, Lichten M (2005) Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169:1353–1367

    Article  PubMed  CAS  Google Scholar 

  • Jones GH (1971) The analysis of exchanges in tritium-labelled meiotic chromosomes. II. Stethophyma grossum. Chromosoma 34:367–382

    Article  Google Scholar 

  • Jones GH, Brumpton RJ (1971) Sister and non-sister chromatid U-type exchange in rye meiosis. Chromosoma 33:115–128

    Article  Google Scholar 

  • Kato H (1977) Spontaneous and induced sister chromatid exchanges as revealed by the BUdR-labeling method. Int Rev Cytol 49:55–97

    Article  PubMed  CAS  Google Scholar 

  • Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1–53

    Article  PubMed  CAS  Google Scholar 

  • 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 143:924–937

    Article  PubMed  CAS  Google Scholar 

  • 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 30:1570–1581

    Article  PubMed  CAS  Google Scholar 

  • Loidl J, Nairz K (1997) Karyotype variability in yeast caused by nonallelic recombination in haploid meiosis. Genetics 146:79–88

    PubMed  CAS  Google Scholar 

  • 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 27:271–276

    Article  PubMed  CAS  Google Scholar 

  • Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454:479–485

    Article  PubMed  CAS  Google Scholar 

  • 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:e1000625

    Article  PubMed  Google Scholar 

  • 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 19:2727–2743

    Article  PubMed  CAS  Google Scholar 

  • Mazrimas JA, Stetka DG (1978) Direct evidence for the role of incorporated BUdR in the induction of sister chromatid exchanges. Exp Cell Res 117:23–30

    Article  PubMed  CAS  Google Scholar 

  • McMahill MS, Sham CW, Bishop DK (2007) Synthesis-dependent strand annealing in meiosis. PLoS Biol 5:e299

    Article  PubMed  Google Scholar 

  • Merker JD, Dominska M, Petes TD (2003) Patterns of heteroduplex formation associated with the initiation of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 165:47–63

    PubMed  CAS  Google Scholar 

  • Michaelis A (1959) Behavior of the ring chromosomes in mitosis and meiosis in Antirrhinum majus L. Chromosoma 10:144–162

    Article  PubMed  CAS  Google Scholar 

  • 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 106:207–215

    Article  PubMed  CAS  Google Scholar 

  • Nag DK, Petes TD (1993) Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol 13:2324–2331

    PubMed  CAS  Google Scholar 

  • Neijzing MG (1982) Chiasma formation in duplicated segments of the haploid rye genome. Chromosoma 85:287–298

    Article  Google Scholar 

  • 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 16:5804–5818

    Article  PubMed  CAS  Google Scholar 

  • 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 36:393–404

    Article  PubMed  CAS  Google Scholar 

  • 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 115:250–259

    Article  PubMed  Google Scholar 

  • 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 144:719–731

    Article  PubMed  CAS  Google Scholar 

  • Peacock WJ (1968) Replication, recombination and chiasmata in Goniaea australasie (Orthoptera, Acrididae). Genetics 65:593–617

    Google Scholar 

  • 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 273:5858–5868

    Article  PubMed  CAS  Google Scholar 

  • 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 275:9390–9395

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Moran E, Santos JL, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev 21:2220–2233

    Article  PubMed  CAS  Google Scholar 

  • Santos JL, Jiménez MM, Díez M (1994) Meiosis in haploid rye: extensive synapsis and low chiasma frequency. Heredity 73:580–588

    Article  Google Scholar 

  • Schwartz D (1953) Evidence for sister-strand crossing over in maize. Genetics 38:251–260

    PubMed  CAS  Google Scholar 

  • 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:e1001190

    Article  PubMed  Google Scholar 

  • Shinohara A, Ogawa H, Ogawa T (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470

    Article  PubMed  CAS  Google Scholar 

  • Smith AV, Roeder GS (1997) The yeast Red1 protein localizes to the cores of meiotic chromosomes. J Cell Biol 136:957–967

    Article  PubMed  CAS  Google Scholar 

  • 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 15:437–451

    Article  PubMed  CAS  Google Scholar 

  • 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 109:35–43

    Article  PubMed  CAS  Google Scholar 

  • Sun H, Treco D, Schultes NP, Szostak JW (1989) Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338:87–90

    Article  PubMed  CAS  Google Scholar 

  • 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 64:1155–1161

    Article  PubMed  CAS  Google Scholar 

  • Taylor JH (1965) Distribution of tritium-labeled DNA among chromosomes during meiosis: I. Spermatogenesis in the grasshopper. J Cell Biol 25:57–68

    Article  PubMed  CAS  Google Scholar 

  • Tease C (1978) Cytological detection of crossing-over in BUdR substituted meiotic chromosomes using the fluorescent plus Giemsa technique. Nature 272:823–824

    Article  PubMed  CAS  Google Scholar 

  • Tease C, Jones GH (1979) Analysis of exchanges in differentially stained meiotic chromosomes of Locusta migratoria after BrdU-substitution and FPG staining. Chromosoma 73:75–84

    Article  Google Scholar 

  • Tease C, Jones GH (1995) Do chiasmata disappear? An examination of whether closely spaced chiasmata are liable to reduction or loss. Chromosome Res 3:162–168

    Article  PubMed  CAS  Google Scholar 

  • 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 38:4349–4360

    Article  PubMed  CAS  Google Scholar 

  • Tsubouchi H, Roeder GS (2006) Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev 20:1766–1775

    Article  PubMed  CAS  Google Scholar 

  • 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 5:385–391

    Article  PubMed  CAS  Google Scholar 

  • 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 106:302–308

    Article  PubMed  CAS  Google Scholar 

  • Viera A, Santos JL, Rufas JS (2009a) Relationship between incomplete synapsis and chiasma localization. Chromosoma 118:377–389

    Article  PubMed  CAS  Google Scholar 

  • 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 118:575–589

    Article  PubMed  CAS  Google Scholar 

  • 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:e1000702

    Article  Google Scholar 

  • Wolff S (1979) Sister chromatid exchange. Ann Rev Genet 11:183–201

    Article  Google Scholar 

  • Wolff S, Perry P (1974) Differential Giemsa staining of sister chromatids and the study of sister chromatid exchanges without autoradiography. Chromosoma 48:341–353

    Article  PubMed  CAS  Google Scholar 

  • 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 188:511–521

    Google Scholar 

  • 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 13:2258–2270

    Article  PubMed  CAS  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to the Ministerio de Ciencia e Innovación of Spain (BFU2008-00459/BMC) and the EU FP7 programme (Meiosys-KBBE-2009-222883) for financial support. We also apologise to all authors whose work could not be cited due to space limitations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mónica Pradillo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pradillo, M., Santos, J.L. The template choice decision in meiosis: is the sister important?. Chromosoma 120, 447–454 (2011). https://doi.org/10.1007/s00412-011-0336-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-011-0336-7

Keywords

Navigation