, Volume 36, Issue 4, pp 343–374 | Cite as

Centromere localization at meiosis and the position of chiasmata in the male and female mouse

  • P. E. Polani


Techniques for obtaining differential Giemsa staining of the paracentromeric (p.c.) regions of male and female mouse meiotic chromosomes (centromeric heterochromatin) were explored and standard procedures developed for the different meiotic cells in the two sexes. The best result followed the use of heat at controlled pH in Sörensen's phosphate buffer or in Standard Saline Citrate (SSC) solutions.

With these techniques, morphological features of the p.c. regions and their variation were studied in normal animals (CFLP strain) and in a strain (AKR) homozygous for a centric fusion [T(11; ?)-1 Ald] between chromosomes No. 6 and No. 15 (Miller et al., 1971). The Y chromosome was often found to show distinct p. c. staining at first and apparently at second meiotic metaphase, and the X and Y chromosomes were found to associate as bivalents by their long arms. Autosomal p.c. regions showed variation in size which might indicate differences between non-homologous chromosomes but a tendency to similarity between homologues. Differences were found between males and females in respect to proportions and variation of bivalents with single and double chiasmata. The relative positions of chiasmata were different in the two sexes. The presence of the centric fusion in the males did not seem to affect the pairing behaviour of the remaining autosomes or of those taking part in the centric fusion. The possibility is discussed that the p.c. regions, to which also other functions would seem to appertain, may be important for chromosome recognition and pairing, possibly on a quantitative basis.


Developmental Biology Relative Position Female Mouse Normal Animal Centric Fusion 
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  1. Arrighi, F. E., Hsu, T. C.: Localization of heterochromatin in human chromosomes. Cytogenetics 10, 81–86 (1971).Google Scholar
  2. Bolton, E. T., McCarthy, B. J.: A general method for the isolation of RNA complementary to DNA. Proc. nat. Acad. Sci. (Wash.) 48, 1390–1397 (1962).Google Scholar
  3. Brinkley, B. R., Stubblefield, E.: The fine structure of the kinetochore of a mammalian cell in vitro. Chromosoma (Berl.) 19, 28–43 (1966).Google Scholar
  4. Brinkley, B. R., Stubblefield, E.: Ultrastructure and interaction of kinetochore and centriole in mitosis and meiosis. In: Advanc. Cell Biol. 1, 119–185 (1970).Google Scholar
  5. Britten, R. J., Kohne, D. E.: Nucleotide sequence repetition in DNA. Carnegie Inst. Wash. Yearbook 65, 78–106 + 123/124 (refs.) (1966).Google Scholar
  6. Britten, R. J., Kohne, D. E.: Repeated sequences in DNA. Science 161, 529–540 (1968).Google Scholar
  7. Britten, R. J., Kohne, D. E.: Repetition of nucleotide sequences in chromosomal DNA. In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), p. 21–36. Amsterdam: North-Holland Publ. Co. 1969.Google Scholar
  8. Cantor, K. P., Hearst, J. E.: The structure of metaphase chromosomes. I. Electrometric titration, magnesium ion binding and circular dichroism. J. molec. Biol. 49, 213–229 (1970).Google Scholar
  9. Chen, A. T. L., Falek, A.: Centromeres in human meiotic chromosomes. Science 166, 1008–1010 (1969).Google Scholar
  10. Chen, T. R., Ruddle, F. H.: Karyotype analysis utilizing differentially stained constitutive heterochromatin of human and murine chromosomes. Chromosoma (Berl.) 34, 51–72 (1971).Google Scholar
  11. Church, K.: Replication of heterochromatin in mouse mammary epithelial cells grown in vitro. Genetics 52, 843–849 (1965).Google Scholar
  12. Comings, D. E.: The rationale for an ordered arrangement of chromatin in the interphase nucleus. Amer. J. hum. Genet. 20, 440–460 (1968).Google Scholar
  13. Comings, D. E., Okada, T. A.: Whole mount electron microscopy of meiotic chromosomes and the synaptonemal complex. Chromosoma (Berl.) 30, 269–286 (1970a).Google Scholar
  14. Comings, D. E., Okada, T. A.: Mechanism of chromosome pairing during meiosis. Nature (Lond.) 227, 451–456 (1970b).Google Scholar
  15. Corneo, G., Ginelli, E., Soave, C., Bernardi, G.: Isolation and characterization of mouse and guinea pig satellite deoxyribonucleic acids. Biochemistry 7, 4373–4379 (1968).Google Scholar
  16. Crick, F.: General model for the chromosomes of higher organisms. Nature (Lond.) 234, 25–27 (1971).Google Scholar
  17. Crouse, H.: The controlling element in sex chromosome behavior in Sciara. Genetics 45, 1429–1443 (1960).Google Scholar
  18. Doty, P., Marmur, J., Eigner, J., Schildkraut, C.: Strand separation and specific recombination in deoxyribonucleic acids: physical chemical studies. Proc. nat. Acad. Sci. (Wash.) 46, 461–476 (1960).Google Scholar
  19. Edwards, R. G.: Meiosis in ovarian oocytes of adult mammals. Nature (Lond.) 196, 446–450 (1962).Google Scholar
  20. Evans, E. P., Breckon, G., Ford, C. E.: An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 3, 289–294 (1964).Google Scholar
  21. Evans, H. J.: Uptake of 3H-thymidine and patterns of DNA replication in nuclei and chromosomes of Vicia faba. Exp. Cell Res. 35, 381–393 (1964).Google Scholar
  22. Flamm, W. G., Bernheim, N. J., Brubaker, P. E.: Density gradient analysis of newly replicated DNA from synchronized mouse lymphoma cells. Exp. Cell Res. 64, 97–104 (1971).Google Scholar
  23. Fogwill, M.: Differences in crossing-over and chromosome size in the sex cells of Lilium and Fritillaria. Chromosoma (Berl.) 9, 493–504 (1958).Google Scholar
  24. Gall, J. G., Pardue, M. L.: Formation and detection of RNA-DNA hybrid molecules in cytological preparations. Proc. nat. Acad. Sci. (Wash.) 63, 378–383 (1969).Google Scholar
  25. Giemsa, G.: Eine Vereinfachung und Vervollkommnung meiner Methylenazur-Methylenblau-Eosin-Färbemethode zur Erzielung der Romanowsky-Nochtschen Chromatinfärbung. Zbl. Bakt., I. Abt. Orig. 37, 308–311 (1904).Google Scholar
  26. Giménez-Martín, G., López-Sáez, J. F., Marcos-Moreno, A.: Structure of the centromere in telocentric chromosomes. Experentia (Basel) 21, 391–392 (1965).Google Scholar
  27. Griffen, A. B.: Mammalian pachytene chromosome mapping and somatic chromosome identification. J. cell. comp. Physiol. 56, 113–121 (1960).Google Scholar
  28. Hall, B. D., Spiegelman, S.: Sequence complementarity of T2-DNA and T2-specific RNA. Proc. nat. Acad. Sci. (Wash.) 47, 137–146 (1961).Google Scholar
  29. Hearst, J. E., Botchan, M.: The eukaryotic chromosome. Ann. Rev. Biochem. 39, 151–182 (1970).Google Scholar
  30. Henderson, S. A.: Chiasma distribution at diplotene in a locust. Heredity 18, 173–190 (1963).Google Scholar
  31. Holliday, R.: Genetic recombination in fungi. In: Replication and recombination of genetic material (W. J. Peacock and R. D. Brock, eds.), p. 157–174. Canberra: Australian Academy of Science 1968.Google Scholar
  32. Hotta, T., Stern, H.: Analysis of DNA synthesis during meiotic prophase in Lilium. J. molec. Biol. 55, 337–355 (1971).Google Scholar
  33. Hsu, T. C., Arrighi, F. E.: Distribution of constitutive heterochromatin in mammalian chromosomes. Chromosoma (Berl.) 34, 243–253 (1971).Google Scholar
  34. Hsu, T. C., Cooper, J. E. K., Mace, M. L., Brinkley, B. R.: Arrangement of centromeres in mouse cells. Chromosoma (Berl.) 34, 73–87 (1971).Google Scholar
  35. John, H. A., Birnstiel, M. L., Jones, K. W.: RNA-DNA hybrids at the cytological level. Nature (Lond.) 223, 582–587 (1969).Google Scholar
  36. Jones, K. W.: Chromosomal and nuclear location of mouse satellite DNA in individual cells. Nature (Lond.) 225, 912–915 (1970).Google Scholar
  37. Jones, K. W., Robertson, F. W.: Localisation of reiterated nucleotide sequences in Drosophila and mouse by in situ hybridisation of complementary RNA. Chromosoma (Berl.) 31, 331–345 (1970).Google Scholar
  38. Kezer, J., MacGregor, H. C.: A fresh look at meiosis and centromeric heterochromatin in the red-backed salamander Plethodon cinereus cinereus (Green). Chromosoma (Berl.) 33, 146–166 (1971).Google Scholar
  39. King, R. C.: Ovarian development in Drosophila melanogaster. New York and London: Academic Press 1970.Google Scholar
  40. Kit, S.: Species differences in animal deoxyribonucleic acids as revealed by equilibrium sedimentation in density gradients. Nature (Lond.) 193, 274–275 (1962).Google Scholar
  41. Kofman-Alfaro, S., Chandley, A. C.: Meiosis in the male mouse. An autoradiographic investigation. Chromosoma (Berl.) 31, 404–420 (1970).Google Scholar
  42. Leonard, A., Deknudt, Gh.: Étude d'une translocation de type Robertsonien chez les souris de race AKR. Acta zool. path. Antverpiensia 48, 43–57 (1969).Google Scholar
  43. Levan, A.: Heterochromaty in chromosomes during their contraction phase. Hereditas (Lund) 32, 449–468 (1946).Google Scholar
  44. Lima-de-Faria, A.: Recent advances in the study of the kinetochore. Int. Rev. Cytol. 7, 123–157 (1958).Google Scholar
  45. Lindegren, C. C., Lindegren, G., Shult, E., Hwang, Y. L.: Centromeres, sites of affinity and gene loci on the chromosomes of Saccharomyces. Nature (Lond.) 194, 260–265 (1962).Google Scholar
  46. Lindsley, D. L., Novitski, E.: Localization of the genetic factors responsible for the kinetic activity of X chromosomes of Drosophila melanogaster. Genetics 43, 790–798 (1958).Google Scholar
  47. Luykx, P.: The structure of the kinetochore in meiosis and mitosis in Urechis eggs. Exp. Cell Res. 39, 643–657 (1965).Google Scholar
  48. Maio, J. J.: DNA strand reassociation and polyribonucleotide binding in the African green monkey, Cercopithecus aethiops. J. molec. Biol. 56, 579–595 (1971).Google Scholar
  49. Maio, J. J., Schildkraut, C. L.: Isolated mammalian metaphase chromosomes. II. Fractionated chromosomes of mouse and Chinese hamster cells. J. molec. Biol. 40, 203–216 (1969).Google Scholar
  50. Marmur, J., Lane, D.: Strand separation and specific recombination in deoxyribonucleic acids: biological studies. Proc. nat. Acad. Sci. (Wash.) 46, 453–461 (1960).Google Scholar
  51. Marmur, J., Rownd, R., Schildkraut, C. L.: Denaturation and renaturation of deoxyribonucleic acid. In: Progress in nucleic acid research (J. N. Davidson and W. E. Cohn, eds.), vol. 1, p. 231–300. New York: Academic Press 1963.Google Scholar
  52. Mather, K.: The determination of position in crossing-over. II. The chromosome length-chiasma frequency relation. Cytologia (Tokyo), Fujii jub. vol., 514–526 (1937).Google Scholar
  53. Meredith, R.: A simple method for preparing meiotic chromosomes from mammalian testis. Chromosoma (Berl.) 26, 254–258 (1969).Google Scholar
  54. Meselson, M., Stahl, F. W., Vinograd, J.: Equilibrium sedimentation of macromolecules in density gradients. Proc. nat. Acad. Sci. (Wash.) 43, 581–589 (1957).Google Scholar
  55. Michie, D.: Affinity: a new genetic phenomenon in the house mouse. Evidence from distant crosses. Nature (Lond.) 171, 26–27 (1953).Google Scholar
  56. Miller, O. J., Miller, D. A., Kouri, R. E., Allderdice, P. W., Dev, V. G., Grewal, M. S., Hutton, J. J.: Identification of the mouse karyotype by quinacrine fluorescence, and tentative assignment of six linkage groups. Proc. nat. Acad. Sci. (Wash.) 68, 1530–1533 (1971).Google Scholar
  57. Monakhova, M. A., Kostenko, A. I.: The dynamics of the relationship between chromosomes and nuclear membrane in the sex cells of the rat. Proc. Acad. Sci. U.S.S.R., biol. Sci. 187, 510–513 (1969).Google Scholar
  58. Odartchenko, N., Pavillard, M.: Late DNA replication in male mouse meiotic chromosomes. Science 167, 1133–1134 (1970).Google Scholar
  59. Ohno, S., Kaplan, W. D., Kinosita, R.: Heterochromatic regions and nucleolus organizers in chromosomes of the mouse, Mus musculus. Exp. Cell Res. 13, 358–364 (1957).Google Scholar
  60. Ohta, T., Kimura, M.: Functional organization of genetic material as a product of molecular evolution. Nature (Lond.) 233, 118–119 (1971).Google Scholar
  61. Pardue, M. L., Gall, J. G.: Molecular hybridization of radioactive DNA to the DNA of cytological preparations. Proc. nat. Acad. Sci. (Wash.) 64, 600–604 (1969).Google Scholar
  62. Pardue, M. L., Gall, J. G.: Chromosomal localization of mouse satellite DNA. Science 168, 1356–1358 (1970).Google Scholar
  63. Rowley, J. D., Bodmer, W. F.: Relationship of centromeric heterochromatin to fluorescent banding patterns of metaphase chromosomes in the mouse. Nature (Lond.) 231, 503–506 (1971).Google Scholar
  64. Schildkraut, C. L., Maio, J. J.: Studies on the intranuclear distribution and properties of mouse satellite DNA. Biochim. biophys. Acta (Amst.) 161, 76–93 (1968).Google Scholar
  65. Schildkraut, C. L., Marmur, J., Doty, P.: The formation of hybrid DNA molecules and their use in studies of DNA homologies. J. molec. Biol. 3, 595–617 (1961).Google Scholar
  66. Schnedl, W.: The karyotype of the mouse. Chromosoma (Berl.) 35, 111–116 (1971).Google Scholar
  67. Schrader, F.: The kinetochore or spindle fibre locus in Amphiuma tridactylum. Biol. Bull. 70, 484–498 (1936).Google Scholar
  68. Southern, E. M.: Base sequence and evolution of guinea-pig α-satellite DNA. Nature (Lond.) 227, 794–798 (1970).Google Scholar
  69. Sumner, A. T., Evans, H. J., Buckland, R. A.: New technique for distinguishing between human chromosomes. Nature (new Biol.) 232, 31–32 (1971).Google Scholar
  70. Sved, J. A.: Telomere attachment of chromosomes. Some genetical and cytological consequences. Genetics 53, 747–756 (1966).Google Scholar
  71. Thomas, C. A.: Recombination of DNA molecules. In: Progress in nucleic acid research and molecular biology (J. N. Davidson and W. E. Cohn, eds.), vol. 5, p. 315–337. New York: Academic Press 1966.Google Scholar
  72. Tobia, A. M., Schildkraut, C. L., Maio, J. J.: Deoxyribonucleic acid replication in synchronized cultured mammalian cells. I. Time of synthesis of molecules of different average guanine + cytosine content. J. molec. Biol. 54, 499–515 (1970).Google Scholar
  73. Ved Brat, S.: Genetic systems in Allium. II. Sex differences in meiosis. In: Chromosomes today (C. D. Darlington and K. R. Lewis, eds.), vol. 1, p. 31–40. Edinburgh and London: Oliver and Boyd 1966.Google Scholar
  74. Walker, P. M. B.: How different are the DNAs from related animals ? Nature (Lond.) 219, 228–232 (1968).Google Scholar
  75. Walker, P. M. B., Flamm, W. G., McLaren, A.: Highly repetitive DNA in rodents. In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), p. 52–66. Amsterdam: North-Holland Publ. Co. 1969.Google Scholar
  76. Wallace, M. E.: Affinity: a new genetic phenomenon in the house mouse. Evidence from within laboratory stocks. Nature (Lond.) 171, 27–28 (1953).Google Scholar
  77. Wallace, M. E.: Affinity: evidence from crossing inbred lines of mice. Heredity 16, 1–23 (1961).Google Scholar
  78. Waring, M. J., Britten, R. J.: Nucleotide sequence repetition: a rapidly reassociating fraction of mouse DNA. Science 154, 791–794 (1966).Google Scholar
  79. Watson, I. D., Callan, H. J.: The form of bivalent chromosomes in newt oocytes at first metaphase of meiosis. Quart. J. micr. Sci. 104, 281–295 (1963).Google Scholar
  80. Williams, C. A., Ockey, C. H.: Distribution of DNA replicator sites in mammalian nuclei after different methods of cell synchronization. Exp. Cell Res. 63, 365–372 (1970).Google Scholar
  81. Woollam, D. H. M., Ford, E. H. R.: The fine structure of the mammalian chromosome in meiotic prophase with special reference to the synaptinemal complex. J. Anat. (Lond.) 98, 163–173 (1964).Google Scholar
  82. Woollam, D. H. M., Ford, E. H. R., Millen, J. W.: The attachment of pachytene chromosomes to the nuclear membrane in mammalian spermatocytes. Exp. Cell Res. 42, 657–661 (1966).Google Scholar
  83. Yunis, J. J., Roldan, L., Yasmineh, W. G., Lee, J. C.: Staining of satellite DNA in metaphase chromosomes. Nature (Lond.) 231, 532–533 (1971).Google Scholar

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© Springer-Verlag 1972

Authors and Affiliations

  • P. E. Polani
    • 1
  1. 1.Paediatric Research UnitGuy's Hospital Medical SchoolLondon

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