Skip to main content
PMC home page
Genetics logoLink to Genetics
. 1999 Apr;151(4):1569–1579. doi: 10.1093/genetics/151.4.1569

Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein.

L K Anderson 1, A Reeves 1, L M Webb 1, T Ashley 1
PMCID: PMC1460565  PMID: 10101178

Abstract

We have used immunofluorescent localization to examine the distribution of MLH1 (MutL homolog) foci on synaptonemal complexes (SCs) from juvenile male mice. MLH1 is a mismatch repair protein necessary for meiotic recombination in mice, and MLH1 foci have been proposed to mark crossover sites. We present evidence that the number and distribution of MLH1 foci on SCs closely correspond to the number and distribution of chiasmata on diplotene-metaphase I chromosomes. MLH1 foci were typically excluded from SC in centromeric heterochromatin. For SCs with one MLH1 focus, most foci were located near the middle of long SCs, but near the distal end of short SCs. For SCs with two MLH1 foci, the distribution of foci was bimodal regardless of SC length, with most foci located near the proximal and distal ends. The distribution of MLH1 foci indicated interference between foci. We observed a consistent relative distance (percent of SC length in euchromatin) between two foci on SCs of different lengths, suggesting that positive interference between MLH1 foci is a function of relative SC length. The extended length of pachytene SCs, as compared to more condensed diplotene-metaphase I bivalents, makes mapping crossover events and interference distances using MLH1 foci more accurate than using chiasmata.

Full Text

The Full Text of this article is available as a PDF (155.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashley T. G-band position effects on meiotic synapsis and crossing over. Genetics. 1988 Feb;118(2):307–317. doi: 10.1093/genetics/118.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker S. M., Plug A. W., Prolla T. A., Bronner C. E., Harris A. C., Yao X., Christie D. M., Monell C., Arnheim N., Bradley A. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet. 1996 Jul;13(3):336–342. doi: 10.1038/ng0796-336. [DOI] [PubMed] [Google Scholar]
  3. Brown S W, Zohary D. The Relationship of Chiasmata and Crossing over in Lilium Formosanum. Genetics. 1955 Nov;40(6):850–873. doi: 10.1093/genetics/40.6.850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carpenter A. T. Electron microscopy of meiosis in Drosophila melanogaster females: II. The recombination nodule--a recombination-associated structure at pachytene? Proc Natl Acad Sci U S A. 1975 Aug;72(8):3186–3189. doi: 10.1073/pnas.72.8.3186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chandley A. C. A model for effective pairing and recombination at meiosis based on early replicating sites (R-bands) along chromosomes. Hum Genet. 1986 Jan;72(1):50–57. doi: 10.1007/BF00278817. [DOI] [PubMed] [Google Scholar]
  6. Egel R. The synaptonemal complex and the distribution of meiotic recombination events. Trends Genet. 1995 Jun;11(6):206–208. doi: 10.1016/s0168-9525(00)89046-0. [DOI] [PubMed] [Google Scholar]
  7. Fang J. S., Jagiello G. A pachytene map of the mouse spermatocyte. Chromosoma. 1981;82(3):437–445. doi: 10.1007/BF00285768. [DOI] [PubMed] [Google Scholar]
  8. Foss E., Lande R., Stahl F. W., Steinberg C. M. Chiasma interference as a function of genetic distance. Genetics. 1993 Mar;133(3):681–691. doi: 10.1093/genetics/133.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fox D. P. The control of chiasma distribution in the locust, Schistocerca gregaria (Forskal). Chromosoma. 1973 Aug 27;43(3):289–328. doi: 10.1007/BF00294277. [DOI] [PubMed] [Google Scholar]
  10. Hale D. W. Is X-Y recombination necessary for spermatocyte survival during mammalian spermatogenesis? Cytogenet Cell Genet. 1994;65(4):278–282. doi: 10.1159/000133648. [DOI] [PubMed] [Google Scholar]
  11. Heng H. H., Tsui L. C., Moens P. B. Organization of heterologous DNA inserts on the mouse meiotic chromosome core. Chromosoma. 1994 Oct;103(6):401–407. doi: 10.1007/BF00362284. [DOI] [PubMed] [Google Scholar]
  12. Holmquist G. P. Evolution of chromosome bands: molecular ecology of noncoding DNA. J Mol Evol. 1989 Jun;28(6):469–486. doi: 10.1007/BF02602928. [DOI] [PubMed] [Google Scholar]
  13. Hultén M. Chiasma distribution at diakinesis in the normal human male. Hereditas. 1974;76(1):55–78. doi: 10.1111/j.1601-5223.1974.tb01177.x. [DOI] [PubMed] [Google Scholar]
  14. Hunter N., Borts R. H. Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev. 1997 Jun 15;11(12):1573–1582. doi: 10.1101/gad.11.12.1573. [DOI] [PubMed] [Google Scholar]
  15. Jagiello G., Fang J. S. Analyses of diplotene chiasma frequencies in mouse oocytes and spermatocytes in relation to ageing and sexual dimorphism. Cytogenet Cell Genet. 1979;23(1-2):53–60. doi: 10.1159/000131302. [DOI] [PubMed] [Google Scholar]
  16. Kaback D. B., Guacci V., Barber D., Mahon J. W. Chromosome size-dependent control of meiotic recombination. Science. 1992 Apr 10;256(5054):228–232. doi: 10.1126/science.1566070. [DOI] [PubMed] [Google Scholar]
  17. King J. S., Mortimer R. K. A polymerization model of chiasma interference and corresponding computer simulation. Genetics. 1990 Dec;126(4):1127–1138. doi: 10.1093/genetics/126.4.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167–8174. doi: 10.1073/pnas.93.16.8167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lawrie N. M., Tease C., Hultén M. A. Chiasma frequency, distribution and interference maps of mouse autosomes. Chromosoma. 1995 Dec;104(4):308–314. doi: 10.1007/BF00352262. [DOI] [PubMed] [Google Scholar]
  20. Lindsley D. L., Sandler L. The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):295–312. doi: 10.1098/rstb.1977.0019. [DOI] [PubMed] [Google Scholar]
  21. Mather K. Crossing over and Heterochromatin in the X Chromosome of Drosophila Melanogaster. Genetics. 1939 Apr;24(3):413–435. doi: 10.1093/genetics/24.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moens P. B., Heyting C., Dietrich A. J., van Raamsdonk W., Chen Q. Synaptonemal complex antigen location and conservation. J Cell Biol. 1987 Jul;105(1):93–103. doi: 10.1083/jcb.105.1.93. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pigozzi M. I., Solari A. J. Extreme axial equalization and wide distribution of recombination nodules in the primitive ZW pair of Rhea americana (Aves, Ratitae). Chromosome Res. 1997 Sep;5(6):421–428. doi: 10.1023/a:1018404610973. [DOI] [PubMed] [Google Scholar]
  24. Polani P. E. Centromere localization at meiosis and the position of chiasmata in the male and female mouse. Chromosoma. 1972;36(4):343–374. doi: 10.1007/BF00336793. [DOI] [PubMed] [Google Scholar]
  25. Poorman P. A., Moses M. J., Davisson M. T., Roderick T. H. Synaptonemal complex analysis of mouse chromosomal rearrangements. III. Cytogenetic observations on two paracentric inversions. Chromosoma. 1981;83(3):419–429. doi: 10.1007/BF00327363. [DOI] [PubMed] [Google Scholar]
  26. Rahn M. I., Solari A. J. Recombination nodules in the oocytes of the chicken, Gallus domesticus. Cytogenet Cell Genet. 1986;43(3-4):187–193. doi: 10.1159/000132319. [DOI] [PubMed] [Google Scholar]
  27. Ried T., Baldini A., Rand T. C., Ward D. C. Simultaneous visualization of seven different DNA probes by in situ hybridization using combinatorial fluorescence and digital imaging microscopy. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1388–1392. doi: 10.1073/pnas.89.4.1388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Roeder G. S. Meiotic chromosomes: it takes two to tango. Genes Dev. 1997 Oct 15;11(20):2600–2621. doi: 10.1101/gad.11.20.2600. [DOI] [PubMed] [Google Scholar]
  29. Scherthan H., Weich S., Schwegler H., Heyting C., Härle M., Cremer T. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol. 1996 Sep;134(5):1109–1125. doi: 10.1083/jcb.134.5.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shaw D. D., Knowles G. R. Comparative chiasma analysis using a computerised optical digitiser. Chromosoma. 1976 Dec 16;59(2):103–127. doi: 10.1007/BF00328480. [DOI] [PubMed] [Google Scholar]
  31. Sherman J. D., Stack S. M. Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics. 1995 Oct;141(2):683–708. doi: 10.1093/genetics/141.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Speed R. M. The effects of ageing on the meiotic chromosomes of male and female mice. Chromosoma. 1977 Nov 30;64(3):241–254. doi: 10.1007/BF00328080. [DOI] [PubMed] [Google Scholar]
  33. Stack S. M. Heterochromatin, the synaptonemal complex and crossing over. J Cell Sci. 1984 Oct;71:159–176. doi: 10.1242/jcs.71.1.159. [DOI] [PubMed] [Google Scholar]
  34. Sybenga J. Recombination and chiasmata: few but intriguing discrepancies. Genome. 1996 Jun;39(3):473–484. doi: 10.1139/g96-061. [DOI] [PubMed] [Google Scholar]
  35. Sym M., Roeder G. S. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell. 1994 Oct 21;79(2):283–292. doi: 10.1016/0092-8674(94)90197-x. [DOI] [PubMed] [Google Scholar]
  36. West S. C. Enzymes and molecular mechanisms of genetic recombination. Annu Rev Biochem. 1992;61:603–640. doi: 10.1146/annurev.bi.61.070192.003131. [DOI] [PubMed] [Google Scholar]
  37. West S. C. The processing of recombination intermediates: mechanistic insights from studies of bacterial proteins. Cell. 1994 Jan 14;76(1):9–15. doi: 10.1016/0092-8674(94)90168-6. [DOI] [PubMed] [Google Scholar]
  38. Wu T. C., Lichten M. Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science. 1994 Jan 28;263(5146):515–518. doi: 10.1126/science.8290959. [DOI] [PubMed] [Google Scholar]
  39. Zickler D., Moreau P. J., Huynh A. D., Slezec A. M. Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics. 1992 Sep;132(1):135–148. doi: 10.1093/genetics/132.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES