Skip to main content
Log in

Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates

  • Original Articles
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Antibodies against human Rad51 protein were used to examine the distribution of Rad51 on meiotic chromatin in mouse spermatocytes and oocytes as well as chicken oocytes during sequential stages of meiosis. We observed the following dynamic changes in distribution of Rad51 during meiosis: (1) in early leptotene nuclei there are multiple apparently randomly distributed, foci that by late leptonema become organized into tracks of foci. (2) These foci persist into zygonema, but most foci are now localized on Rad51-positive axes that correspond to lateral elements of the synaptonemal complex. As homologs synapse foci from homologous axes fuse. The distribution and involvement of Rad51 foci as contact points between homologs suggest that they may be components to early recombination nodules. (3) As pachynema progresses the number of foci drops dramatically; the temporal occurrence (mice) and physical and numerical distribution of foci on axes (chickens) suggest that they may be a component of late recombination nodules. (4) In early pachynema there are numerous Rad51 foci on the single axis of the X (mouse spermatocytes) or the Z (chiken oocytes) chromosomes that neither pair, nor recombine. (5) In late pachynema in mouse spermatocytes, but not oocytes, the Rad51 signal is preferentially enhanced at both ends of all the bivalents. As bivalents in spermatocytes, but not oocytes, begin to desynapse at diplonema they are often held together at these Rad51-positive termini. These observations parallel observations that recombination rates are exceptionally high near chromosome ends in male but not female eutherian mammals. (6) From diakinesis through metaphase I, Rad51 protein is detected as low-intensity fluorescent doublets that localize with CREST-specific antigens (kinetochores), suggesting that Rad51 participates, at least as a structural component of the materials involved, in sister kinetochore cohesiveness. Finally, the changes in Rad51 distribution during meiosis do not appear to be species specific, but intrinsic to the meiotic process.

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.

Institutional subscriptions

Similar content being viewed by others

References

  • Albini SM, Jones GH (1987) Synaptonemal complex spreading in Alium cepa and A. fistulosum. I. The initiation and sequence of pairing. Chromosoma 95: 324–338

    Google Scholar 

  • Allen JW, Latt SA (1976) In vivo BrdU-33258 Hoechst analysis of DNA replication kinetics and sister chromatid exchange formation in mouse somatic and meiotic cells. Chromosoma 58: 325–340

    Google Scholar 

  • Anderson LK, Stack SM (1988) Nodules associated with axial cores and synaptonemal complexes during zygotene in Psilotum nudum Chromosoma 97: 96–100

    Google Scholar 

  • Ashley T (1994) Mammalian meiotic recombination: a reexamination. Hum Genet 94: 587–593

    Google Scholar 

  • Bezzubova O, Shinohara A, Mueller RG, Ogawa H, Buerstedde JM (1993) A chicken RAD51 homologue is expressed at high levels in lymphoid and reproductive organs. Nucleic Acids Res 21: 1577–1580

    Google Scholar 

  • Bishop DK (1994) RecA homologues DMC 1 and RAD51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081–1092

    Google Scholar 

  • Bishop DK, Park D, Xu L, Kleckner N (1992) DMC1: a meiotic specific yeast homolog of E. coli. recA required for recombination, synaptonemal complex formation and cell cycle progression. Cell 69: 439–456

    Google Scholar 

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

    Google Scholar 

  • Carpenter ATC (1979) Recombination nodules and synaptonemal complex in recombination-defective females of Drosophila melanogaster. Chromosoma 75: 259–292

    Google Scholar 

  • Carpenter ATC (1981) EM autoradiographic evidence that DNA synthesis occurs at recombination nodules during meiosis in Drosophila melanogaster females. Chromosoma 83: 59–80

    Google Scholar 

  • Carpenter ATC (1987) Gene conversion, recombination nodules, and the initiation of meiotic synapsis. BioEssays 6: 232–236

    Google Scholar 

  • Chandley AC, McBeath S (1987) DNase I hypersensitive sites along the XY bivalen at meiosis in man include the XpYp pairing region. Cytogenet Cell Genet 44: 22–31

    Google Scholar 

  • Dietrich AJJ, de Boer P (1983) A sequential analysis of the development of the synaptonemal complex in spermatocytes of the mouse by electron microscopy using hydroxyurea and agar filtration. Genetica 61: 119–129

    Google Scholar 

  • Dietrich AJJ, Mulder PJP (1983) A light and electron microscopic analysis of meiotic prophase in female mice. Chromosoma 88: 377–385

    Google Scholar 

  • Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulous B, Moens PB (1994) Synaptonemal complex proteins, epitope mapping and chromosome disjunction. J Cell Sci 107: 2749–2760

    Google Scholar 

  • Friedberg EC (1988) Deoxyribonucleic acid repair in the yeast Saccaromyces cerevisiae. Microbiol Rev 52: 70–102

    Google Scholar 

  • Goetz P, Chandley AC, Speed RM (1984) Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse. J Cell Sci 65: 249–263

    Google Scholar 

  • Haaf T, Golub EI, Reddy G, Radding CM, Ward DC (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92: 2298–2302

    Google Scholar 

  • Jachymczyk WJ, von Borstel RC, Mowat MRA, Hastings PJ (1981) Repair of interstrand cross-links in DNA of Saccharomyces cerevisiae requires two systems for DNA repair: the RAD3 system and the RAD51 system. Mol Gen Genet 182: 196–205

    Google Scholar 

  • Kaelbling M, Fechheimer NS (1983) Synaptonemal complexes and the chromosome component of dometic fowl, Gallus domesticus. Cytogenet Cell Genet 35: 87–92

    Google Scholar 

  • Kleckner N, Padmore R, Bishop DK (1991) Meiotic chromosome metabolism: one coherent view. Cold Spring Harbor Symp Quant Biol 56: 729–743

    Google Scholar 

  • Maguire MP (1993) Sister chromatid association at meiosis. Maydica 38: 93–106

    Google Scholar 

  • McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71–80

    Google Scholar 

  • Moens PB, Heyting C, Dietrich AJJ, van Raamsdonk W, Chen Q (1987) Synaptonemal complex antigen localization and conservation. J Cell Biol 105: 93–103

    Google Scholar 

  • Moses MJ (1980) New cytogenetic studied on mammalian meiosis. In: Serio M, Martini L (eds) Animal models in human reproduction. Raven Press, New York, pp 169–190

    Google Scholar 

  • Moses MJ, Dresser ME, Poorman PA (1984) Composition and role of the synaptonemal complex. Symp Soc Exp Biol 38: 245–270

    Google Scholar 

  • Nicolas A, Petes TD (1994) Polarity of meiotic gene conversion in fungi: contrasting views. Experimentia 50: 242–252

    Google Scholar 

  • Ogawa T, Shinohara A, Nabetan A, Ikeya T, Yu X, Egelman EH, Ogawa H (1993a) RecA-like recombination proteins in eukaryotes: functions and structures of Rad51 genes. Cold Spring Harbor Symp Quant Biol 58: 569–576

    Google Scholar 

  • Ogawa T, Xiong Y, Shinohara A, Egelman EH (1993b) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259: 1896–1899

    Google Scholar 

  • Padmore R, Cao L, Kleckner N (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239–1256

    Google Scholar 

  • Petes TD, Malone RE, Syminton LS (1992) Recombination in yeast. In: Broach JR, Pringle J, Jones E (eds) The molecular and cellular biology of the yeast Saccharomyces. Genome dynamics, protein synthesis, and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 407–521

    Google Scholar 

  • Radding CM (1988) Homologous pairing and strand exchange promoted by Escherichia coli RecA protein. In: Kucherlapati R, Smith GR (eds) Genetic recombination. American Society for Microbiology Washington, DC, pp 193–229

    Google Scholar 

  • Radding CM (1991) Helical interactions in homologous pairing and strand exchange driven by RecA protein. J Biol Chem 266: 5355–5358

    Google Scholar 

  • Rahn MI, Solari AJ (1986) Recombination nodules in the oocyte of the chicken, Gallus domesticus. Cytogenet Cell Genet 43: 187–193

    Google Scholar 

  • Richler C, Uliel E, Kemen B-S, Wahrman J (1987) Regions of active chromatin conformation in “inactive” male meiotic sex chromosomes of the mouse. Chromosoma 95:165–170

    Google Scholar 

  • Ried T, Baldini A, Rand T, Ward DC (1992) Simultaneous visualization of seven different DNA probes by in situ hybridization using, combinatorial fluorescence and digital imaging microscopy. Proc Natl Acad Sci USA 89:1388–1392

    Google Scholar 

  • Roeder GS (1990) Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends Genet 6:385–389

    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

    Google Scholar 

  • Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human mouse and fission yeast recombination genes homologous to Rad51 and recA. Nature Genet 4:239–243

    Google Scholar 

  • Solari AJ (1970) The behavior of the chromosomal axes during diplotene in mouse spermatocytes. Chromosoma 31:217–230

    Google Scholar 

  • Solari AJ (1970) Ultrastructure of the synaptic autosomes and the ZW bivalent in chicken oocytes. Chromosoma 64:155–165

    Google Scholar 

  • Solari AJ (1979) Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae; Hemiptera). Chromosoma 72:225–240

    Google Scholar 

  • Speed RM (1982) Meiosis in the foetal ovary I: An analysis at the light microscope level using surface spreading. Chromosoma 85:427–437

    Google Scholar 

  • Stern H, Hotta Y (1987) The biochemistry of meiosis. In: Moens PB (ed) Meiosis. Academic Press, New York, pp 303–331

    Google Scholar 

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

    Google Scholar 

  • Terasawa M, Shinohara A, Hotta Y, Ogawa H, Ogawa T (1995) Localization of RecA-like recombination proteins on chromosomes of lily at various meiotic stages. Genes and Dev 9925–934

    Google Scholar 

  • Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitital interactions before and during meiosis in yeast. Cell 77:977–991

    Google Scholar 

  • Zickler D, Moreau PJ; Huyh AD, Slezec AM (1992) Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics 132:135–148

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ashley, T., Plug, A.W., Xu, J. et al. Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates. Chromosoma 104, 19–28 (1995). https://doi.org/10.1007/BF00352222

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00352222

Keywords

Navigation