Skip to main content
NCBI home page
American Journal of Human Genetics logoLink to American Journal of Human Genetics
. 1994 Sep;55(3):423–430.

Multipoint linkage map of the human pseudoautosomal region, based on single-sperm typing: do double crossovers occur during male meiosis?

K Schmitt 1, L C Lazzeroni 1, S Foote 1, D Vollrath 1, E M Fisher 1, T M Goradia 1, K Lange 1, D C Page 1, N Arnheim 1
PMCID: PMC1918414  PMID: 8079986

Abstract

Sperm typing was used to measure recombination fractions among pseudoautosomal markers and the beginning of the X/Y-specific sequences located at the pseudoautosomal boundary. These experiments included primer-extension preamplification and PCR followed by allele typing using gel electrophoresis. A newly developed data-analysis program allowed the construction of the first multipoint-linkage sperm-typing map, using results obtained on seven loci from three individuals. The large sample size not only confirmed the increased recombination activity of the pseudoautosomal region but allowed an estimate of interference of recombination to be made. The coefficient of coincidence was calculated to be .26 over a physical distance of only approximately 1,800 kb. The observation of a few sperm presumably resulting from double recombination argues that more than one crossover event can occur in this region during male meiosis.

Full text

PDF
423

Selected References

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

  1. Arveiler B., Vincent A., Mandel J. L. Toward a physical map of the Xq28 region in man: linking color vision, G6PD, and coagulation factor VIII genes to an X-Y homology region. Genomics. 1989 May;4(4):460–471. doi: 10.1016/0888-7543(89)90269-3. [DOI] [PubMed] [Google Scholar]
  2. Brown W. R. A physical map of the human pseudoautosomal region. EMBO J. 1988 Aug;7(8):2377–2385. doi: 10.1002/j.1460-2075.1988.tb03082.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burgoyne P. S. Genetic homology and crossing over in the X and Y chromosomes of Mammals. Hum Genet. 1982;61(2):85–90. doi: 10.1007/BF00274192. [DOI] [PubMed] [Google Scholar]
  4. Chandley A. C., Goetz P., Hargreave T. B., Joseph A. M., Speed R. M. On the nature and extent of XY pairing at meiotic prophase in man. Cytogenet Cell Genet. 1984;38(4):241–247. doi: 10.1159/000132070. [DOI] [PubMed] [Google Scholar]
  5. Cooke H. J., Brown W. R., Rappold G. A. Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature. 1985 Oct 24;317(6039):687–692. doi: 10.1038/317687a0. [DOI] [PubMed] [Google Scholar]
  6. Cui X. F., Li H. H., Goradia T. M., Lange K., Kazazian H. H., Jr, Galas D., Arnheim N. Single-sperm typing: determination of genetic distance between the G gamma-globin and parathyroid hormone loci by using the polymerase chain reaction and allele-specific oligomers. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9389–9393. doi: 10.1073/pnas.86.23.9389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ellis N. A., Goodfellow P. J., Pym B., Smith M., Palmer M., Frischauf A. M., Goodfellow P. N. The pseudoautosomal boundary in man is defined by an Alu repeat sequence inserted on the Y chromosome. Nature. 1989 Jan 5;337(6202):81–84. doi: 10.1038/337081a0. [DOI] [PubMed] [Google Scholar]
  8. Foote S., Vollrath D., Hilton A., Page D. C. The human Y chromosome: overlapping DNA clones spanning the euchromatic region. Science. 1992 Oct 2;258(5079):60–66. doi: 10.1126/science.1359640. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Freije D., Helms C., Watson M. S., Donis-Keller H. Identification of a second pseudoautosomal region near the Xq and Yq telomeres. Science. 1992 Dec 11;258(5089):1784–1787. doi: 10.1126/science.1465614. [DOI] [PubMed] [Google Scholar]
  12. Goradia T. M., Stanton V. P., Jr, Cui X. F., Aburatani H., Li H. H., Lange K., Housman D. E., Arnheim N. Ordering three DNA polymorphisms on human chromosome 3 by sperm typing. Genomics. 1991 Jul;10(3):748–755. doi: 10.1016/0888-7543(91)90459-r. [DOI] [PubMed] [Google Scholar]
  13. Hassold T. J., Sherman S. L., Pettay D., Page D. C., Jacobs P. A. XY chromosome nondisjunction in man is associated with diminished recombination in the pseudoautosomal region. Am J Hum Genet. 1991 Aug;49(2):253–260. [PMC free article] [PubMed] [Google Scholar]
  14. Henke A., Fischer C., Rappold G. A. Genetic map of the human pseudoautosomal region reveals a high rate of recombination in female meiosis at the Xp telomere. Genomics. 1993 Dec;18(3):478–485. doi: 10.1016/s0888-7543(11)80003-0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Lange K., Weeks D., Boehnke M. Programs for Pedigree Analysis: MENDEL, FISHER, and dGENE. Genet Epidemiol. 1988;5(6):471–472. doi: 10.1002/gepi.1370050611. [DOI] [PubMed] [Google Scholar]
  18. Lazzeroni L. C., Arnheim N., Schmitt K., Lange K. Multipoint mapping calculations for sperm-typing data. Am J Hum Genet. 1994 Sep;55(3):431–436. [PMC free article] [PubMed] [Google Scholar]
  19. Li H. H., Gyllensten U. B., Cui X. F., Saiki R. K., Erlich H. A., Arnheim N. Amplification and analysis of DNA sequences in single human sperm and diploid cells. Nature. 1988 Sep 29;335(6189):414–417. doi: 10.1038/335414a0. [DOI] [PubMed] [Google Scholar]
  20. Mohandas T. K., Speed R. M., Passage M. B., Yen P. H., Chandley A. C., Shapiro L. J. Role of the pseudoautosomal region in sex-chromosome pairing during male meiosis: meiotic studies in a man with a deletion of distal Xp. Am J Hum Genet. 1992 Sep;51(3):526–533. [PMC free article] [PubMed] [Google Scholar]
  21. Morton N. E., Collins A. Standard maps of chromosome 10. Ann Hum Genet. 1990 Jul;54(Pt 3):235–251. doi: 10.1111/j.1469-1809.1990.tb00381.x. [DOI] [PubMed] [Google Scholar]
  22. Page D. C., Bieker K., Brown L. G., Hinton S., Leppert M., Lalouel J. M., Lathrop M., Nystrom-Lahti M., de la Chapelle A., White R. Linkage, physical mapping, and DNA sequence analysis of pseudoautosomal loci on the human X and Y chromosomes. Genomics. 1987 Nov;1(3):243–256. doi: 10.1016/0888-7543(87)90051-6. [DOI] [PubMed] [Google Scholar]
  23. Page D. C., Brown L. G., de la Chapelle A. Exchange of terminal portions of X- and Y-chromosomal short arms in human XX males. 1987 Jul 30-Aug 5Nature. 328(6129):437–440. doi: 10.1038/328437a0. [DOI] [PubMed] [Google Scholar]
  24. Pascoe L., Morton N. E. The use of map functions in multipoint mapping. Am J Hum Genet. 1987 Feb;40(2):174–183. [PMC free article] [PubMed] [Google Scholar]
  25. Petit C., Levilliers J., Weissenbach J. Physical mapping of the human pseudo-autosomal region; comparison with genetic linkage map. EMBO J. 1988 Aug;7(8):2369–2376. doi: 10.1002/j.1460-2075.1988.tb03081.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Renwick J. H. Progress in mapping human autosomes. Br Med Bull. 1969 Jan;25(1):65–73. doi: 10.1093/oxfordjournals.bmb.a070673. [DOI] [PubMed] [Google Scholar]
  27. Riles L., Dutchik J. E., Baktha A., McCauley B. K., Thayer E. C., Leckie M. P., Braden V. V., Depke J. E., Olson M. V. Physical maps of the six smallest chromosomes of Saccharomyces cerevisiae at a resolution of 2.6 kilobase pairs. Genetics. 1993 May;134(1):81–150. doi: 10.1093/genetics/134.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rouyer F., Simmler M. C., Johnsson C., Vergnaud G., Cooke H. J., Weissenbach J. A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature. 1986 Jan 23;319(6051):291–295. doi: 10.1038/319291a0. [DOI] [PubMed] [Google Scholar]
  29. Saiki R. K., Bugawan T. L., Horn G. T., Mullis K. B., Erlich H. A. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature. 1986 Nov 13;324(6093):163–166. doi: 10.1038/324163a0. [DOI] [PubMed] [Google Scholar]
  30. Schmitt K., Vollrath D., Foote S., Fisher E. M., Page D. C., Arnheim N. Four PCR-based polymorphisms in the pseudoautosomal region of the human X and Y chromosomes. Hum Mol Genet. 1993 Nov;2(11):1978–1978. doi: 10.1093/hmg/2.11.1978. [DOI] [PubMed] [Google Scholar]
  31. Shields D. C., Collins A., Buetow K. H., Morton N. E. Error filtration, interference, and the human linkage map. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6501–6505. doi: 10.1073/pnas.88.15.6501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Simmler M. C., Johnsson C., Petit C., Rouyer F., Vergnaud G., Weissenbach J. Two highly polymorphic minisatellites from the pseudoautosomal region of the human sex chromosomes. EMBO J. 1987 Apr;6(4):963–969. doi: 10.1002/j.1460-2075.1987.tb04846.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Simmler M. C., Rouyer F., Vergnaud G., Nyström-Lahti M., Ngo K. Y., de la Chapelle A., Weissenbach J. Pseudoautosomal DNA sequences in the pairing region of the human sex chromosomes. Nature. 1985 Oct 24;317(6039):692–697. doi: 10.1038/317692a0. [DOI] [PubMed] [Google Scholar]
  34. Slim R., Le Paslier D., Compain S., Levilliers J., Ougen P., Billault A., Donohue S. J., Klein D. C., Mintz L., Bernheim A. Construction of a yeast artificial chromosome contig spanning the pseudoautosomal region and isolation of 25 new sequence-tagged sites. Genomics. 1993 Jun;16(3):691–697. doi: 10.1006/geno.1993.1249. [DOI] [PubMed] [Google Scholar]
  35. Soriano P., Keitges E. A., Schorderet D. F., Harbers K., Gartler S. M., Jaenisch R. High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7218–7220. doi: 10.1073/pnas.84.20.7218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Speed R. M., Chandley A. C. Prophase of meiosis in human spermatocytes analysed by EM microspreading in infertile men and their controls and comparisons with human oocytes. Hum Genet. 1990 May;84(6):547–554. doi: 10.1007/BF00210808. [DOI] [PubMed] [Google Scholar]
  37. Vollrath D., Foote S., Hilton A., Brown L. G., Beer-Romero P., Bogan J. S., Page D. C. The human Y chromosome: a 43-interval map based on naturally occurring deletions. Science. 1992 Oct 2;258(5079):52–59. doi: 10.1126/science.1439769. [DOI] [PubMed] [Google Scholar]
  38. Wapenaar M. C., Petit C., Basler E., Ballabio A., Henke A., Rappold G. A., van Paassen H. M., Blonden L. A., van Ommen G. J. Physical mapping of 14 new DNA markers isolated from the human distal Xp region. Genomics. 1992 May;13(1):167–175. doi: 10.1016/0888-7543(92)90217-g. [DOI] [PubMed] [Google Scholar]
  39. Weissenbach J., Levilliers J., Petit C., Rouyer F., Simmler M. C. Normal and abnormal interchanges between the human X and Y chromosomes. Development. 1987;101 (Suppl):67–74. [PubMed] [Google Scholar]
  40. Yen P. H., Marsh B., Allen E., Tsai S. P., Ellison J., Connolly L., Neiswanger K., Shapiro L. J. The human X-linked steroid sulfatase gene and a Y-encoded pseudogene: evidence for an inversion of the Y chromosome during primate evolution. Cell. 1988 Dec 23;55(6):1123–1135. doi: 10.1016/0092-8674(88)90257-7. [DOI] [PubMed] [Google Scholar]
  41. Zhang L., Cui X., Schmitt K., Hubert R., Navidi W., Arnheim N. Whole genome amplification from a single cell: implications for genetic analysis. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5847–5851. doi: 10.1073/pnas.89.13.5847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. de la Chapelle A. The etiology of maleness in XX men. Hum Genet. 1981;58(1):105–116. doi: 10.1007/BF00284157. [DOI] [PubMed] [Google Scholar]

Articles from American Journal of Human Genetics are provided here courtesy of American Society of Human Genetics

RESOURCES