Skip to main content
SpringerLink
Log in

Ultrastructural analysis of maize pachytene karyotypes by three dimensional reconstruction of the synaptonemal complexes

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Aldehyde fixation followed by staining with phosphotungstic acid produces differential contrast between the synaptonemal complex and the chromatin of maize pachytene bivalents. Centromeres, heterochromatic knobs and large chromomeres are easily recognised. With this and other staining techniques the nucleolus organizer region can be differentiated into two components. — Microsporocyte nuclei at pachytene were serially sectioned and all ten bivalents reconstructed in five nuclei. An idiogram was derived from the mean chromosome (= synaptonemal complex) lengths, the arm ratios, positions of knobs and the nucleolus organizer region. The idiogram agrees well with that published from light microscopic analyses. However, bivalent lengths are only two thirds of those observed by light microscopy of squash preparations. Many telomeres of the bivalents are connected via chromatin to the nuclear envelope, but a varying number of free bivalent ends are observed in all five reconstructed nuclei. — Bivalents heterozygous for inversion 3b were reconstructed. In the presence of abnormal chromosome 10 (K10) the lateral components of the synaptonemal complex of chromosome 3 formed a typical inversion loop, while in one of the nuclei having no K10 the two lateral components of the long arms of chromosome 3 remained unpaired in the region of inversion heterozygosity. The presence of K10, which increases crossing-over frequencies and promotes intimate pairing at the light microscopic level, was thus found to permit formation of complete synaptonemal complexes in the inverted region. The extra terminal portion of the K10 chromosome folded back on itself and formed a morphologically normal synaptonemal complex in this — possibly non-homologously paired — region. The chromatin of centromeres and knobs from different bivalents were sometimes found to fuse, but the synaptonemal complexes transversing the fused centromeres or knobs retained their individuality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

  • Bajer, A., Molè-Bajer, J.: Formation of spindle fibers, kinetochore orientation, and behaviour of the nuclear envelope during mitosis in endosperm. Fine structural and in vitro studies. Chromosoma (Berl.) 27, 448–484 (1969)

    Google Scholar 

  • Bernhard, W.: A new staining procedure for electron microscopical cytology. J. Ultrastruct. Res. 27, 250–265 (1969)

    Google Scholar 

  • Berns, M. W., Cheng, W. K.: Are chromosomes' secondary constrictions nucleolus organizers? A re-examination using a laser microbeam. Exp. Cell Res. 69, 185–192 (1971)

    Google Scholar 

  • Brady, T., Clutter, M. E.: Cytolocalization of ribosomal cistrons in plant polytene chromosomes. J. Cell Biol. 53, 827–832 (1972)

    Google Scholar 

  • Braselton, J. P., Bowen, C. C.: The ultrastructure of the kinetochores of Lilium longiflorum during the first meiotic division. Caryologia (Firenze) 24, 49–58 (1971a)

    Google Scholar 

  • Braselton, J. P., Bowen, C. C.: The fine structure of the nucleolus organizers of Lilium longiflorum during meiosis. Cytologia (Tokyo) 36, 529–533 (1971b)

    Google Scholar 

  • Brinkley, B. R., Stubblefield, E.: Ultrastructure and interaction of the kinetochore and centriole in mitosis and meiosis. Advanc. Cell Biol. 1, 119–185 (1970)

    Google Scholar 

  • Das, N. K.: Inactivation of the nucleolar apparatus during meiotic prophase in corn anthers. Exp. Cell Res. 40, 360–364 (1965)

    Google Scholar 

  • Dietrich, J.: Organisation ultrastructurale du fuseau de caryocinèse en prométaphase dans les cellules-mères de microspores du Lis. C. R. Acad. Sci. (Paris), Ser. D 266, 579–581 (1968).

    Google Scholar 

  • Esponda, P., Giménez-Martín, G.: The attachment of the synaptonemal complex to the nuclear envelope. An ultrastructural and cytochemical analysis. Chromosoma (Berl.) 38, 405–417 (1972a)

    Google Scholar 

  • Esponda, P., Giménez-Martín, G.: Ultrastructural morphology of the nucleolar organizing region. J. Ultrastruct. Res. 39, 509–519 (1972b)

    Google Scholar 

  • Esponda, P., Stockert, J. C.: Localization of RNA in the synaptinemal complex. J. Ultrastruct. Res. 35, 411–417 (1971)

    Google Scholar 

  • Galey, F. R., Nilsson, S. E. G.: A new method for transferring sections from the liquid surface of the trough through staining solution to the supporting film of a grid. J. Ultrastruct. Res. 14, 405–410 (1966)

    Google Scholar 

  • Gillies, C. B.: Reconstruction of the Neurospora crassa pachytene karyotype from serial sections of synaptonemal complexes. Chromosoma (Berl.) 36, 119–130 (1972)

    Google Scholar 

  • Gillies, C. B.: Methods for electron microscopic study of maize pachytene chromosomes. Maize Genetics Coop. News Letter 47 (in press, 1973)

  • Gillies, C. B., Hyde, B. B.: Intranucleolar bodies in maize pachytene microsporocytes. Hereditas (Lund) 74 (in press, 1973)

  • Grell, R. F., Bank, H., Gassner, G.: Meiotic exchange without the synaptinemal complex. Nature (Lond.) New Biol. 240, 155–157 (1972)

    Google Scholar 

  • Gurgel, J. A.: The non-homologous associations of centromeres and knobs of maize chromosomes at meiosis. Maize Genetics Coop. News Letter 30, 54–57 (1956)

    Google Scholar 

  • Hsu, T. C., Brinkley, B. R., Arrighi, F. E.: The structure and behaviour of the nucleolus organizers in mammalian cells. Chromosoma (Berl.) 23, 137–153 (1967)

    Google Scholar 

  • 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 

  • Jones, K. W.: Chromosomal and nuclear location of mouse satellite DNA in individual cells. Nature (Lond.) 225, 912–915 (1970).

    Google Scholar 

  • La Cour, L. F., Wells, B.: The chromomeres of pre-pachytene chromosomes. Cytologia (Tokyo) 36, 111–120 (1971)

    Google Scholar 

  • La Cour, L. F., Wells, B.: Deformed lateral elements in synaptonemal complexes of Phaedranassa viridiflora. Chromosoma (Berl.) 41, 289–296 (1973)

    Google Scholar 

  • Lima-de-Faria, A., Sarvella, P.: Variation of the chromosome phenotype in Zea, Solanum and Salvia. Chromosoma (Berl.) 13, 300–314 (1962).

    Google Scholar 

  • McClintock, B.: The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z. Zellforsch. 21, 294–328 (1934)

    Google Scholar 

  • McLeish, J., Sunderland, N.: Measurements of deoxyribonucleic acid (DNA) in higher plants by Feulgen photometry and chemical means. Exp. Cell Res. 24, 527–540 (1961)

    Google Scholar 

  • Menzel, M. Y., Price, J. M.: Fine structure of synapsed chromosomes in F1 Lycopersicon esculentum — Solanum lycopersicoides and its parents. Amer. J. Bot. 53, 1079–1086 (1966)

    Google Scholar 

  • Miller, O. L., Beatty, B. R.: Visualization of nucleolar genes. Science 164, 955–957 (1969)

    Google Scholar 

  • Moens, P. B.: The structure and function of the synaptinemal complex in Lilium longiflorum sporocytes. Chromosoma (Berl.) 23, 418–451 (1968a)

    Google Scholar 

  • Moens, P. B.: Synaptinemal complexes of Lilium tigrinum (triploid) sporocytes. Canad. J. Genet. Cytol. 10, 799–807 (1968b)

    Google Scholar 

  • Moens, P. B.: The fine structure of meiotic chromosome pairing in the triploid Lilium tigrinum. J. Cell Biol. 40, 273–279 (1969)

    Google Scholar 

  • Moens, P. B.: Serial sectioning in electron microscopy. Proc. Canad. Fed. Biol. Soc. 13, 160 (1970a)

    Google Scholar 

  • Moens, P. B.: The fine structure of meiotic chromosome pairing in natural and artificial Lilium polyploids. J. Cell Sci. 7, 55–63 (1970b)

    Google Scholar 

  • Moens, P. B., Perkins, F. O.: Chromosome number of a small protist: Accurate determination. Science 166, 1289–1291 (1969)

    Google Scholar 

  • Moses, M. J.: Synaptonemal complex. Ann. Rev. Genetics 2, 363–412 (1968)

    Google Scholar 

  • Nebel, B. R., Coulon, E. M.: The fine structure of chromosomes in pigeon spermatocytes. Chromosoma (Berl.) 13, 272–291 (1962)

    Google Scholar 

  • Neuffer, M. G., Jones, L., Zuber, M. S.: The mutants of maize, 74 pp. Madison, Wisc.: Crop Science Society of America 1968

    Google Scholar 

  • Parchman, L. G., Lin, K. C.: Nucleolar RNA synthesis during meiosis of lily microsporocytes. Nature (Lond.) New Biol. 239, 235–237 (1972)

    Google Scholar 

  • Pardue, M. L., Gerbi, S. A., Eckhardt, R. A., Gall, J. G.: Cytological localization of DNA complementary to ribosomal RNA in polytene chromosomes of Diptera. Chromosoma (Berl.) 29, 268–290 (1970)

    Google Scholar 

  • Phillips, R. L., Kleese, R. A., Wang, S. S.: The nucleolus organizer region of maize (Zea mays L.): Chromosomal site of DNA complementary to ribosomal RNA. Chromosoma (Berl.) 36, 79–88 (1971)

    Google Scholar 

  • Rhoades, M. M.: Preferential segregation in maize. Genetics 27, 395–407 (1942)

    Google Scholar 

  • Rhoades, M. M.: Meiosis in maize. J. Hered. 41, 58–67 (1950)

    Google Scholar 

  • Rhoades, M. M.: Studies on the cytological basis of crossing over. In: Replication and recombination of genetic material (W. J. Peacock and R. D. Brock, eds.), pp. 229–241. Canberra: Australian Acad. Science 1968

    Google Scholar 

  • Rhoades, M. M., Dempsey, E.: The effect of abnormal chromosome 10 on preferential segregation and crossing over in maize. Genetics 53, 989–1020 (1966)

    Google Scholar 

  • Roth, T. F., Parchman, L. G.: Alteration of meiotic chromosomal pairing and synaptonemal complexes by cycloheximide. Chromosoma (Berl.) 35, 9–27 (1971)

    Google Scholar 

  • Sen, S. K.: Synaptonemal complexes in haploid Petunia and Antirrhinum sp. Naturwissenschaften 57, 550 (1970)

    Google Scholar 

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

    Google Scholar 

  • Solari, A. J.: The spatial relationship of the X and Y chromosomes during meiotic prophase in mouse spermatocytes. Chromosoma (Berl.) 29, 217–236 (1970)

    Google Scholar 

  • Solari, A. J.: The behaviour of chromosomal axes in Searle's X-autosome translocation. Chromosoma (Berl.) 34, 99–112 (1971)

    Google Scholar 

  • Ting, Y. C.: Fine structure of the meiotic first prophase chromosomes in haploid and diploid maize. Genetics 61, 58 (1969)

    Google Scholar 

  • Underbrink, A. G., Ting, Y. C., Sparrow, A. H.: Note on the occurrence of a synaptinemal complex at meiotic prophase in Zea mays L. Canad. J. Genet. Cytol. 9, 606–609 (1967).

    Google Scholar 

  • Walters, M. S.: A nuclear body in microsporocytes of Zea mays. Chromosoma (Berl.) 17, 78–84 (1965)

    Google Scholar 

  • Weber, D. F., Alexander, D. E.: Redundant segments in Zea mays detected by translocations of monoploid origin. Chromosoma (Berl.) 39, 27–42 (1972)

    Google Scholar 

  • Westergaard, M., Wettstein, D. von: The synaptinemal complex. Ann. Rev. Genet. 6, 71–110 (1972)

    Google Scholar 

  • Wettstein, R., Sotelo, J. R.: Electron microscope serial reconstruction of the spermatocyte I nuclei at pachytene. J. Microscopie 6, 557–576 (1967).

    Google Scholar 

  • Wilson, H. J.: The fine structure of the kinetochore in meiotic cells of Tradescantia. Planta (Berl.) 78. 379–385 (1968)

    Google Scholar 

  • Zickler, D.: Fine structure of chromosome pairing in the Ascomycetes: Meiotic and premeiotic (mitotic) synaptonemal complexes. Chromosoma (Berl.) 40, 401–416 (1973)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Carlsberg Laboratory, Denmark

    C. B. Gillies

  2. Department of Genetics, University of Copenhagen, Denmark

    C. B. Gillies

Authors
  1. C. B. Gillies
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gillies, C.B. Ultrastructural analysis of maize pachytene karyotypes by three dimensional reconstruction of the synaptonemal complexes. Chromosoma 43, 145–176 (1973). https://doi.org/10.1007/BF00483376

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00483376

Keywords

Search

Navigation