Skip to main content
Log in

Hierarchy of organization in eukaryotic chromosomes (a review)

  • Published:
Acta Biotheoretica Aims and scope Submit manuscript

Summary

Several models of macromolecular arrangements in eukaryotic chromosomes have been proposed during the past fifteen years. Many of the models are consistent with physical and chemical data on the molecular components of chromosomes, and a few have the appearance of meeting the requirements for cytological organization in chromosomes. However, one of the most frustrating problems in developing a working model is to provide a scheme that fits genetic function while satisfying the structural parameters. This has not yet been achieved.

Although emphasis in this review has been placed on uninemic and polynemic models, alternatives, such as a bineme, for example, remain. It is clear, moreover, that the issue can be resolved only through continued efforts to make direct observations of chromosomes with light and electron microscopy coupled with the additional tools ofX-ray analysis and analytical biochemistry. A recent analysis byWray andStubblefield (1969) has led to a rather innovative model of the chromosome, and exemplifies the kind of approach needed to clarify the phenomenon. Furthermore, analyses of meiotic chromosomes may provide valuable insight for relating organization to genetic function (cf Maguire, 1966 andBraselton, pers. comm). Of particular interest are mutation events as related to subchromatid organization, and the reorganization of chromosomal fibrils during early meiotic stages. At present, and as a generalization, the evidence points more strongly toward at least a binemic arrangement of chromosomal subunits than toward a uninemic one.

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

  • Abuelo, J. G. andD. E. Moore (1969). “The human chromosome,”J. Cell Biol. 41: 73–90.

    Google Scholar 

  • Alfert, M. andW. Balamuth (1957). “Differential micronuclear polyteny in a population of the ciliateTetrahymena pyriformisChromosoma 8: 371–379.

    Google Scholar 

  • Anderson, T. (1951). “Techniques for the preservation of three-dimensional structure in preparing specimens for the electron microscope”-Trans. N.Y. Acad. Sci. II, 13: 130–134.

    Google Scholar 

  • Auerbach, C. (1951). “Problems in chemical mutagenesis”-Cold Spr. Harb. Symp. Quant. Biol. 16: 199–213.

    Google Scholar 

  • Bajer, A. (1965). “Subchromatid structure of chromosomes in the living state”-Chromosoma 17: 291–312.

    Google Scholar 

  • Bastia, D. andM. S. Swaminathan (1967). “Ultrastructure of interphase chromosomes”-Exptl. Cell Research 48: 18–26.

    Google Scholar 

  • Brinkley, B. R. and M. W.Shaw (1968). “A comparative light and electron microscope study of human chromosomes”-Genetics Soc. of Amer. abstracts, p. 165.

  • — andR. M. Humphrey (1969). “Evidence for subchromatid organization in marsupial chromosomes. I. Light and electron microscopy of X-ray-induced sidearm bridges”-J. Cell Biology 42: 827–836.

    Google Scholar 

  • Brooke, J. H., D. P. Jenkins, R. K. Lawson, andE. E. Osgood (1962). “Human chromosome uncoiling and dissociation”-Ann. Human Genet. 26: 139–156.

    Google Scholar 

  • Callan, H. G. (1967). “The organization of genetic units in chromosomes”-J. Cell Sci. 2: 1–7.

    Google Scholar 

  • Christenhuss, R., Th. Buchner, andR. A. Pfeiffer (1967). “Visualization of human somatic chromosomes by scanning electron microscopy”-Nature 216: 379–380.

    Google Scholar 

  • Comings, D. E. andT. A. Okada (1969). “Electron microscope study of well dispersed mammalian and avian chromosomes: A single DNA helix per chromatid model,”J. Cell Biol. 43: 25a-26a (abstract).

    Google Scholar 

  • Crouse, H. V. (1954). “X-ray breakage of lily chromosomes at first meiotic metaphase,”Science 119: 485–487.

    Google Scholar 

  • — (1961). “Irradiation of condensed meiotic chromosomes inLilium longiflorum,”Chromosoma 12: 190–214.

    Google Scholar 

  • Dales, S. (1960). “A study of the fine structure of mammalian somatic chromosomes,”Exptl. Cell Research 19: 577–590.

    Google Scholar 

  • Darlington, C. D. (1955). “The chromosome as a physico-chemical entity,”Nature 176: 1139–1144.

    Google Scholar 

  • — andA. Haque, (1969). “The replication and division of polynemic chromosomes,”Heredity 24: 273–280.

    Google Scholar 

  • Dounce, A. L. andC. A. Hilgartner (1965). “A study of DNA nucleoprotein gels and the residual protein of isolated cell nuclei. Relationship to chromosomal structure,”Exptl. Cell Research 36: 228–241.

    Google Scholar 

  • DuPraw, E. J. (1965). “The organization of nuclei and chromosomes in honeybee embryonic cells,”Proc. Natl. Acad. Sci. U.S. 53: 161–168.

    Google Scholar 

  • — (1966). “Evidence for a “Folded Fibre” organization in human chromosomes,”Nature 209: 577–581.

    Google Scholar 

  • — andG. F. Bahr (1969). “The arrangement of DNA in human chromosomes, as investigated by quantitative electron microscopy,”Acta Cytologica 13: 188–205.

    Google Scholar 

  • Fox D. P. (1966). “The effects ofX-rays on the chromosomes of locust embryos. I. The early responses,”Chromosoma 19: 300–316.

    Google Scholar 

  • Gall, J. G. (1963a). “Kinetics of deoxyribonuclease action on chromosomes,”Nature 198: 36–38.

    Google Scholar 

  • — (1963b). “Chromosome fibers from an interphase nucleus,”Science 139: 120–121.

    Google Scholar 

  • — andH. F. Callan (1962). “H3-uridine incorporation in lampbrush chromosomes,”Proc. Natl. Acad. Sci. U.S. 48: 562–570.

    Google Scholar 

  • Gimenez-Martin, G. andJ. F. Lopez-Saez (1963). “Somatic chromosome structure (Observations with the light microscope),”Cytologia 28: 381–389.

    Google Scholar 

  • Gimenez-Martin, G. andJ. F. Lopez-Saez (1965). “Chromosome structure in the course of mitosis,”Cytologia 30: 14–22.

    Google Scholar 

  • Govaerts, A. andD. Dekegel (1966), “Electron micrography of human chromosomes,”Nature 209: 831–832.

    Google Scholar 

  • Halkka, O. (1964). “A photometric study of theLuzula problem,”-Hereditas 52: 81–88.

    Google Scholar 

  • Heddle, J. A. M. (1968). “Chromosome structure in Newts,”Radiat. Research 35: 521–522. (abstract).

    Google Scholar 

  • Heddle, J. A. andJ. E. Trosko (1966). “Is the transition from chromosome to chromatid aberrations the result of the formation of single-stranded DNA ?”Exptl. Cell Research 42: 171–177.

    Google Scholar 

  • — andD. J. Bodycote (1968). “The strandedness of chromosomes,”J. Cell Biol. 39: 60a (abstract).

    Google Scholar 

  • — — “The strandedness of lampbrush chromosomes,”J. Cell Biol. 43: 52a (abstract).

    Google Scholar 

  • Hsu, T. C., W. C. Dewey, andR. M. Humphrey (1962). “Radiosensitivity of cells of Chinese hamster in vitro in relation to the cell cycle,”Exptl. Cell Research 27: 441–452.

    Google Scholar 

  • Hughes-Schrader, S. (1940). “The meiotic chromosomes of the maleLlaveiella taenechnia Morrison (Coccoidae) and the question of the tertiary split,”-Biol. Bull. 78: 312–337.

    Google Scholar 

  • Humphrey, R. M. andB. R. Brinkley (1969). “Ultrastructural studies of radiation-induced chromosome damage,”-J. Cell Biol. 42: 745–753.

    Google Scholar 

  • Ito, M., Y. Hotta, andH. Stern (1967). “Studies of meiosis in vitro. II. Effect of inhibiting DNA synthesis during meiotic prophase on chromosome structure and behavior,”Developmental Biology 6: 54–77.

    Google Scholar 

  • Kaufmann, B. P. (1926). “Chromosome structure and its relation to the chromosome cycle. I. Somatic mitosis inTradescantia pilosa,”-Amer. J. Botany 13: 59–80.

    Google Scholar 

  • — (1931). “Chromonemata in somatic and meiotic mitoses,”Amer. Naturalist 65: 289–293.

    Google Scholar 

  • — andN. D. De (1956). “Fine structure of chromosomes,”J. Biophys. Biochem. Cytol. 2(suppl.) 419–423.

    Google Scholar 

  • —,H. Gay, andM. R. McDonald (1960). “Organizational patterns within chromosomes,”Intern. Rev. Cytology 9: 77–128.

    Google Scholar 

  • Kihlman, B. A. andB. Hartley (1967). “Sub-chromatid exchanges and the “Folded fibre” model of chromosome structure,”Hereditas 57: 289–294.

    Google Scholar 

  • Kleinschmidt, A. K., D. Lang, C. Plescher, W. Hellman, J. Haass, R. K. Zahn, andA. Hagedorn (1961). “Über die intra-zellulare Formation von bakterien-DNS,”Z. Naturforsch. 16 b: 730–739.

    Google Scholar 

  • —,D. Lang, D. Jacherts, andR. K. Zahn (1962). “Darstellung und Langenmessungen des gesamten Desoxyribonucleinsaure-inhaltes von T2 bakteriophagen,”Biophys. Biochem. Acta 61: 857–864.

    Google Scholar 

  • Kuwada, Y. (1939). “Chromosome structure. A critical review,”-Cytologia 10: 213–256.

    Google Scholar 

  • LaCour, L. F. andA. Rutishauser (1954). “X-ray breakage experiments with endosperm. I. Sub-chromatid breakage.”Chromosoma 6: 696–709.

    Google Scholar 

  • — andS. R. Pelc (1958). “Effect of colchicine on the utilization of labeled thymidine during chromosomal reproduction,”Nature 182: 506–508.

    Google Scholar 

  • Luzzati, V. andA. Nicolaieff (1963). “The structure of nucleohistones and nucleoprotamines,”J. Molecular Biology 7: 142–163.

    Google Scholar 

  • McClintock, B. (1938). “The fusion of broken ends of sister half-chromatids following chromatid breakage at meiotic anaphases,”Missouri Agric. Exp. Sta. Res. Bull. 290: 1–48.

    Google Scholar 

  • McDermott, A. (1969). “Chromosome fine structure: electron microscopy of unfixed, negatively stained human chromosomes,”Cytologia 33: 397–400.

    Google Scholar 

  • Maguire, M. P. (1966). “Double-strandedness of meiotic prophase chromatids to light microscope optics and its relationship to genetic recombination,”Proc. Natl. Acad. Sci. U.S. 55: 44–50.

    Google Scholar 

  • — (1968). “Nomarski interference contrast resolution of sub-chromatid structure,”Proc. Natl. Acad. Sci. U.S. 60: 533–536.

    Google Scholar 

  • Manton, I. (1945). “New evidence on the telophase split inTodea barbara,”-Amer. J. Botany 32: 342–348.

    Google Scholar 

  • Martin, P. G. andR. Shanks (1966). “DoesVicia faba have multi-stranded chromosomes,”-Nature 211: 650–651.

    Google Scholar 

  • Miller, O. L., Jr. (1965). “Fine Structure of Lampbrush Chromosomes,”Natl. Cancer Inst. Monograph 18: 79–99.

    Google Scholar 

  • Moses, M. J. (1968). “Synaptinemal complex”Ann. Rev. Genet. 2: 363–412.

    Google Scholar 

  • Nebel, B.R. (1939). “Chromosome structure,”Botan. Rev. 5: 563–626.

    Google Scholar 

  • Osgood, E. E., D. P. Jenkins, R. Brooks, andR. K. Lawson (1964). “Electron micrographic studies of the expanded and uncoiled chromosomes from human leukocytes,”Ann. N.Y. Acad. Sci. 113: 717–726.

    Google Scholar 

  • Ostergren, G. andT. Wakonig (1954). “True or apparent sub-chromatid breakage and the induction of labile states in cytological chromosome loci,”Bot. Notiser 4: 357–375.

    Google Scholar 

  • Pardon, J. F., M. H. F. Wilkins, andB. M. Richards (1967). “Super-helical model for nucleohistone,”Nature 215: 508–509.

    Google Scholar 

  • Peacock, W. J. (1961). “Sub-chromatid structure and chromosome duplication inVicia faba,”-Nature 191: 832–833.

    Google Scholar 

  • — (1963). “Chromosome duplication and structure as determined by autoradiography,”Proc. Natl. Acad. Sci. U.S. 49: 793–801.

    Google Scholar 

  • Prescott, D. M. andM. A. Bender (1963). “Autoradiographic study of chromatid distribution of labeled DNA in two types of mammalian cells in vitro,”Exptl. Cell Research 29: 430–442.

    Google Scholar 

  • Ris H. (1954). “The submicroscopic structure of chromosomes,”Leiden Symposium on Fine Structure of Cells.

  • - (1966a). “The organization of chromosomal nucleohistone fibrils,”Sixth Intern. Congr. for Electron Microscopy, Kyoto. 339–340.

  • — (1966b). “Fine structure of chromosomes,”Proc. Roy. Soc., B, 164: 246–257.

    Google Scholar 

  • — (1967). “Ultrastructure of the animal chromosome,” in:V.V. Koningsberger andL. Bosch (eds.),Regulation of Nucleic Acid and Protein Biosynthesis, pp. 11–21, Elsevier, Amsterdam.

    Google Scholar 

  • — (1968). “Effect of fixation on the dimension of nucleohistone fibers,”J. Cell Biol. 39: 158a (abstract).

    Google Scholar 

  • Rothfels, K., E. Sexsmith, M. Heimburger, andM. O. Krause, (1966). “Chromosome size and DNA content of species ofAnemone L. and related genera (Ranunculaceae),”Chromosoma 20: 54–74.

    Google Scholar 

  • Schrader, F. andS. Hughes-Schrader (1956). “Polyploidy and fragmentation in the chromosomal evolution of various species ofThyanta (Hemiptera),”-Chromosoma 7: 469–496.

    Google Scholar 

  • — andS. Hughes-Schrader (1958). “Chromatid autonomy inBanasa (Hemiptera: Pentatomidae),”Chromosoma 9: 193–215.

    Google Scholar 

  • Solari, A. J. (1965). “Structure of the chromatin in sea urchin sperm,”Proc. Natl. Acad. Sci. U.S., 53: 503–511.

    Google Scholar 

  • — (1968a). “The ultrastructure of chromatin fibers. I. The effect of spreading conditions,”Exptl. Cell Research 53: 553–566.

    Google Scholar 

  • — (1968b). “The ultrastructure of chromatin fibers. II. The ultrastructure of the loops from sea urchin sperm chromatin,”Exptl. Cell Research 53: 567–581.

    Google Scholar 

  • Sparvoli, E., H. Gay, andB. P. Kaufmann (1965). “Number and pattern of association of chromonemata in the chromosomes ofTradescantia,”Chromosoma 16: 415–435.

    Google Scholar 

  • Steffensen, D. (1959). “A comparative view of the chromosome,”Brookhaven Symposia in Biology 12: 103–124.

    Google Scholar 

  • — (1961). “Chromosome structure with special reference to the role of metal ions,”Intern. Rev. Cytol. 12: 163–197.

    Google Scholar 

  • Stern, H. andY. Hotta (1969). “DNA synthesis in relation to chromosome pairing and chiasma formation,”Genetics 61: 27–40.

    Google Scholar 

  • Stockert, J. C., (1969). “Presence of sub-chromatids in Murine chromosomes,”Cytologia 33: 200–201.

    Google Scholar 

  • Swanson C. P. (1947). “X-ray and ultraviolet studies on pollen type chromosomes. II. The quadripartite structure of the prophase chromosome ofTradescantia,”Proc. Natl. Acad. Sci. U.S. 33: 229–232.

    Google Scholar 

  • — (1957). Cytology and Cytogenetics,-Prentice-Hall, Inc., Englewood Cliffs, N. J.

    Google Scholar 

  • Swift, H. (1967). “Molecular morphology of the chromosome,” in:C. J. Dawe, ed., The Chromosome I, In Vitro, p. 26–49,-Williams and Wilkins Co., Balt. Md.

    Google Scholar 

  • Taylor, J. H. (1958). “Sister chromatid exchanges in tritium-labeled chromosomes,”Genetics 43: 515–529.

    Google Scholar 

  • —,P. S. Woods, andW. L. Hughes (1957). “The organization and duplication of chromosomes as revealed by autoradiographic studies using tritium labeled thymidine,”Proc. Natl. Acad. Sci. U.S. 43: 122–138.

    Google Scholar 

  • Trosko, J. E. andS. Wolff (1965). “Strandedness ofVicia faba chromosomes as revealed by enzyme digestion studies,”-J. Cell Biol. 26: 125–135.

    Google Scholar 

  • — andJ. G. Brewen (1966). “Cytological observation on the strandedness of mammalian metaphase chromosomes,”-Cytologia 31: 208–212.

    Google Scholar 

  • Uhl, C. (1965). “Chromosome structure and crossing over,”Genetics 51: 191–207.

    Google Scholar 

  • Vosa, C. G. (1968). “A method to reveal sub-chromatids in somatic chromosomes,”Caryologia 21: 381–383.

    Google Scholar 

  • Walen, K. (1965). “Spatial relationships in the replication of chromosomal DNA,”Genetics 51: 915–929.

    Google Scholar 

  • Wilkins, M. H. F. (1956). “Molecular structure of deoxyribose nucleic acid and nucleoprotein and possible implications in protein synthesis,”Biochem. Soc., London, Symp. 14: 13–27.

    Google Scholar 

  • Wolfe, S. L. (1968). “The effect of prefixation on the diameter of chromosome fibers isolated by the Langmuir trough-critical point method,”J. Cell Biol. 37: 610–620.

    Google Scholar 

  • — andB. John (1965). “The organization and ultrastructure of male meiotic chromosomes inOncopeltus fasciatus,”Chromosoma 7: 85–103.

    Google Scholar 

  • — andN. J. Grim (1967). “The relationship of isolated chromosome fibers to the fibers of the embedded nucleus,”J. Ultrastruct. Research 19: 382–397.

    Google Scholar 

  • — andP.G. Martin (1968). “The ultrastructure and strandedness of chromosomes from two species ofVicia,”Exptl. Cell Research 50: 140–150.

    Google Scholar 

  • Wolff, S. (1965). “On the chemistry of chromosome continuity,”National Cancer Inst. Monogr. 18: 155–180.

    Google Scholar 

  • — (1969a). “Strandedness of chromosomes,”Intern. Rev. Cytol. 25: 279–296

    Google Scholar 

  • — (1969b.) “The splitting of human chromosomes in chromatids in the absence of either DNA or protein synthesis,”Mutation Research 8: 207–214.

    Google Scholar 

  • Wray, W. andE. Stubblefield (1969). “Separation and biochemical analysis of the morphological components of mammalian chromosomes,”J. Cell Biol. 43: 160a (abstract).

    Google Scholar 

  • Zubay, G. (1964). “Nucleohistone structure and function,” in:J. Bonner andP. Ts'o, eds., The Nucleohistones—Holden-Day, San Francisco.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cohn, N.S. Hierarchy of organization in eukaryotic chromosomes (a review). Acta Biotheor 20, 41–70 (1971). https://doi.org/10.1007/BF01556968

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01556968

Keywords

Navigation