Skip to main content
Log in

An ‘axis-like’ material in the centromeric region of metaphase-I chromosomes from mouse spermatocytes

  • Research Article
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

This study reports the persistence of axis-like structures in the centromeric region of both homologues during the metaphase-I and anaphase-I stages of meiotic division of mouse spermatocytes. A novel type of silver ‘argentaffin’ technique (NH4−Ag) is employed. This technique includes the treatment of glutaraldehyde-fixed tissues with dilute ammonium hydroxide followed by a reduction of aldehyde groups with sodium borohydride. Staining is accomplished with ammoniacal silver nitrate in darkness followed by sulfite washing. The lateral elements of synaptonemal complexes and the single chromosomal axes of diplotene spermatocytes show a prominent reactivity with this technique. The pattern of very small grains over condensed chromatin is uniform and gives only a light opacity to the electron beam. The presence of an axis-like structure is seen in every centromeric end of meiotic chromosomes at metaphase I and anaphase I. The chromatin (heterochromatin) that surrounds the centromeric filament and some material distributed in irregular linear arrays along some of the homologues also showed a higher electron opacity than the bulk of deoxyribonucleoprotein. While the former is related to C+ heterochromatin, the latter could represent dispersed material of diplotene axes. It is suggested that the disposal of axial material is differentially delayed at the centromeric regions. The present evidence supports the hypothesis that axial fragments or lateral-element segments persisting at these regions contribute to the cohesiveness of centromeres of sister chromatids during normal disjunction.

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.

Similar content being viewed by others

References

  • Dresser, M. E. & Moses, M. J., 1980. Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). IV. Light and electron microscopy of synapsis and nucleolar development by silver staining. Chromosoma 76: 1–22.

    Google Scholar 

  • Earnshaw, W. C. & Laemmli, U. K., 1984. Silver staining of the chromosome scaffold. Chromosoma 89: 186–192.

    Google Scholar 

  • Gallyas, F., 1982. Physico-chemical mechanism of the argyrophil I reaction. Histochemistry 74: 393–407.

    Google Scholar 

  • Gautier, H., 1976. Ultrastructural localization of DNA in ultrathin tissue sections. Int. Rev. Cytol. 44: 114–191.

    Google Scholar 

  • Heyting, C., Dettmers, R. J., Dietrich, A. J. J., Redecker, J. W. & Vink, A. C. G., 1988. Two major components of synaptonemal complexes are specific for meiotic prophase nuclei. Chromosoma 96: 325–332.

    Google Scholar 

  • Howell, W. M., 1982. Selective staining of nucleolus organizing regions (NORs), vol XI, pp. 89–141. In: The Cell Nucleus, edited by H.Busch and L.Rothblum. Academic Press Inc., New York.

    Google Scholar 

  • Jimenez-Garcia, L. F., Rothblum, L. I., Busch, H. & Ochs, R. L., 1989. Nucleologenesis: use of non-isotopic in situ hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis. Biol. Cell 65: 239–246.

    Google Scholar 

  • Knibiehler, B., Mirre, C., Hartung, M., Jean, P. & Stahl, A. 1981. Sex-vesicle-associated nucleolar organizers in mouse spermatocytes: localization, structure sand function. Cytogenet. Cell Genet. 31: 47–57.

    Google Scholar 

  • Lillie, R. D. & Pizzolato, P., 1972. Histochemical use of borohydrides as aldehyde blocking agents. Stain Technol. 47: 13–17.

    Google Scholar 

  • Luykx, P., 1974. The organization of meiotic chromosomes pp. 163–207. In: The Cell Nucleus, edited by H.Busch, Vol. II. Academic Press, New York.

    Google Scholar 

  • Maguire, M. P., 1974. The need for a chiasma binder. J. theor. Biol. 48: 485–487.

    Google Scholar 

  • Maguire, M. P., 1978. A possible role for the synaptonemal complex in chiasma maintenance. Exptl. Cell Res. 112: 297–308.

    Google Scholar 

  • Moens, P. B., 1969. Multiple core complexes in grasshopper spermatocytes and spermatids. J. Cell Biol. 40: 542–551.

    Google Scholar 

  • Moens, P. B. & Church, K., 1979. The distribution of synaptonemal complex material in metaphase I bivalents of Locusta and Chlolealtis. (Orthoptera:Acrididae). Chromosoma 73: 247–254.

    Google Scholar 

  • Moses, M. J., 1977. The synaptonemal complex and meiosis, pp. 101–125. In: Molecular Human Cytogenetics, edited by R. S.Sparkes, D. E.Comings and D. F.Fox, Academic Press, New York.

    Google Scholar 

  • Moses, M. J., Dresser, M. E. & Poorman, P., 1984. Composition and role of the SC, pp. 245–270. In: Controlling events in meiosis, edited by C. W.Evans and H. G.Dickerson, Vol. 3. The Company of Biologists, Cambridge, U.K.

    Google Scholar 

  • Nicklas, R. B., 1961. Recurrent pole to pole movements of the sex chromosome during prometaphase-I in Melanoplus differentialis spermatocytes. Chromosoma 12: 97–115.

    Google Scholar 

  • Nicklas, R. B., 1988. Chromosomes and kinetochores do more in mitosis than previously thought, in Chromosome Structure and Function, edited by J. P.Gustafson and R.Appels, pp. 53–74, Plenum Publishing Corp., New York.

    Google Scholar 

  • Ochs, R. L., Lischwe, M. A., Shen, E., Carrol, R. E. & Busch, H., 1985. Nucleologenesis: composition and fate of prenucleolar bodies. Chromosoma 92: 330–336.

    Google Scholar 

  • Rieder, C. L., 1982. The formation, structure and composition of the mammalian kinetochore and kinetochore fiber. Int. Rev. Cytol. 79: 1–58.

    Google Scholar 

  • Risueno, M. C., Testillano, P. S., Ollacarizqueta, M. A. & Tandler, C. J., 1990. The ‘argentaffin’ reaction of the nucleolus. Silver reducing sites after mercuric acetate and copper tetrammine treatments, in Nuclear Structure and Function, edited by J. R.Harris, and I. B.Zbarsky. Plenum Press, New York, in the press.

    Google Scholar 

  • Rufas, J. S., Gimenez-Martin, G. & Esponda, P., 1982. Presence of a chromatid core in mitotic and meiotic chromosomes of grasshoppers. Cell Biol. Int. Reports 6: 261–267.

    Google Scholar 

  • Rufas, J. S., Gimenez-Abian, J., Suja, J. A., and Garcia de la Vega, C., 1987. Chromosome organization in meiosis revealed by light microscope analysis of silver-stained cores. Genome 29: 706–712.

    Google Scholar 

  • Sheridan, W. F. & Barrnett, R. J., 1969. Cytochemical studies on chromosome ultrastructure. J. Ultrastruct. Res. 27: 216–229.

    Google Scholar 

  • Solari, A. J., 1969. The evolution of the ultrastructure of the sex chromosomes (sex vesicle) during meiotic prophase in mouse spermatocytes. J. Ultrastruct. Res. 27: 67–75.

    Google Scholar 

  • Solari, A. J., 1970. The behavior of chromosomal axes during diplotene in mouse spermatocytes. Chromosoma 31: 217–230.

    Google Scholar 

  • Solari, A. J., 1974. The relationship between chromosomes and axes in the chiasmatic XY pair of the Armenian hamster (Cricetulus migratorius). Chromosoma 48: 89–106.

    Google Scholar 

  • Solari, A. J., 1979. Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae; Hemiptera). Chromosoma 81: 315–337.

    Google Scholar 

  • Solari, A. J., 1981. Chromosomal axes during and after diplotene, pp. 178–186, in International Cell Biology 1980–1981, edited by H. G.Schweiger. Springer-Verlag, Berlin.

    Google Scholar 

  • Solari, A. J. & Ashley, T., 1977. Ultrastructure and behavior of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus). Chromosoma 62: 319–336.

    Google Scholar 

  • Solari, A. J. & Counce, S. J., 1977. Synaptonemal complex karyotyping in Melanoplus differentialis. J. Cell Sci. 26: 229–250.

    Google Scholar 

  • Tandler, C. J., 1959. The silver-reducing property of the nucleolus and the formation of prenucleolar material during mitosis. Exptl. Cell Res. 17: 560–564.

    Google Scholar 

  • Tandler, C. J. & Pellegrino de Iraldi, A., 1989. A silver-reducing component in rat striated muscle. I. Selective localization at the level of the terminal-cistern/transverse tubule system. Histochemistry 92: 15–22.

    Google Scholar 

  • Tandler, C. J., Gonzalez, D. A., Remorini, P. G. & Pellegrino de Iraldi, A., 1989. A silver-reducing component in rat striated muscle. II. Isolated sarcoplasmic reticulum. Histochemistry 92: 23–27.

    Google Scholar 

  • Tandler, C. J. & Pellegrino de Iraldi, A., 1990. Staining terminal cisternae proteins in rat skeletal muscle triads: selectivity of a new silver technique, in Electron Microscopy 1990, edited by L. D.Peachey and D. B.Williams. San Francisco Press Inc., San Francisco, vol. 3: 736–737.

    Google Scholar 

  • Wettstein, D. v., Rasmussen, S. W. & Holm, P. B., 1984. The synaptonemal complex in genetic segregation. Ann. Rev. Genet. 18: 331–413.

    Google Scholar 

  • Westergaard, M. & vonWettstein, D., 1970. Studies on the mechanism of crossing-over. IV. The molecular organization of the synaptinemal complex in Neotiella (Cooke) Saccardo (Ascomycetes). C. R. Trav. Lab. Carlsberg 37: 239–268.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tandler, C.J., Solari, A.J. An ‘axis-like’ material in the centromeric region of metaphase-I chromosomes from mouse spermatocytes. Genetica 84, 39–49 (1991). https://doi.org/10.1007/BF00123983

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00123983

Keywords

Navigation