Abstract
The Dinoflagellate Prorocentrum micans has been studied in classical and high voltage transmission electron microscopy, with the help of a goniometric stage. The general structure of the nucleus is analysed with special reference to the links observed between chromosomes and the nuclear envelope, the nucleoplasm and the nucleolus. The chromosomes present stacked series of nested arcs which are studied in detail. The sense of the arcs can be changed by a simple tilt of the section. These arcs do not correspond to DNA filaments with a genuine bend but to an illusion created by the overlap of layers of filaments whose orientation turns along the chromosome axis. — The transversal orientation of DNA and the examination of defects allow to rule out the polytenic hypothesis. It is clear that this hypothesis does not apply to bacterial nucleoids, which however can form series of nested arcs as in Dinoflagellate chromosomes. — The twisted arrangement of Dinoflagellate chromosomes is that of a liquid crystal of the cholesteric type. DNA is known to self assemble into cholesteric phases and this affords informations on the origin of the elongated shape of chromosomes and on the mechanisms of condensation and aggregation observed in this particular chromatin.
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Allen, J.R., Roberts, T.M., Loeblich, A.R. III, Klotz, L.C.: Characterization of the DNA from the Dinoflagellate Crypthecodinium cohnii and implications for nuclear organization. Cell 6, 161–169 (1975)
Babillot, C.: Etude de l'incorporation d'uridine tricié dans le noyau d'Amphidinium carteri (Dinoflagellé). C.R. Acad. Sci. (Paris) 271, 838–841 (1970)
Beam, C.A., Himes, M.: Evidence for sexual fusion and recombination in the Dinoflagellate Crypthecodinium (Gyrodinium) cohnii. Nature (Lond.) 250, 435–436 (1974)
Bouligand, Y.: Sur une architecture torsadée répandue dans de nombreuses cuticules d'Arthropodes. C.R.Acad. Sci. (Paris) 261, 3665–3668 (1965)
Bouligand, Y.: Sur l'existence de “pseudomorphoses cholesteriques” chez divers organismes vivants. J. de Physique C 4 30, Suppl. 11–12, 90–103 (1969)
Bouligand, Y.: Twisted fibrous arrangement in biological materials and cholesteric mesophases. Tissue and Cell 4, 189–217 (1972)
Bouligand, Y.: Recherches sur les textures des états mésomorphes. 5. Noyaux, fils et rubans de Moebius dans les nématiques et les cholestériques peu torsadés. J. de Physique 35, 315–236 (1974)
Bouligand, Y.: Cholesteric order in Biopolymers. Polymer preprints (A.C.S.) 18, 33–38 (1977)
Bouligand, Y.: Liquid crystalline order in biological materials. In: Liquid crystalline order in polymers (A. Blumstein, ed.), pp. 261–297. New York, London: Academic Press 1978a
Bouligand, Y.: Liquid crystals and their analogs in biological systems. Solid State Physics 34, 259–294 (1978b)
Bouligand, Y., Soyer, M.O., Puiseux-Dao, S.: La structure fibrillaire et l'orientation des chromosomes chez les Dinoflagellés. Chromosoma 24, 251–287 (1968a)
Bouligand, Y., Soyer, M.O., Puiseux-Dao, S.: Liaisons morphologiquement définies entre chromosomes et membrane nucléaire chez certains Péridiniens. C.R. Acad. Sci. (Paris) 266, 1287–1289 (1968b)
Bouteille, M., Laval, M., Dupuy-Coin, A.M.: Localization of nuclear functions as revealed by ultrastructural autoradiography and cytochemistry. In: The cell nucleus (H. Busch, ed.) vol. 1, p. 22–30. New York: Academic Press 1974
Darlington, C.D.: Recent advances in cytology. London: Churchill 1937
Dodge, J.D.: Chromosome structure in the Dinophyceae. II Cytochemical studies. Arch. Microbiol. 48, 66–80 (1964)
Dodge, J.D.: The Dinophyceae. In: The chromosomes of the algae. (M.B.E. Godward, ed.) pp. 96–115 London: E. Arnold 1966
Elliot, G.F., Rome, E.M.: Liquid crystalline aspects of muscle fibers. Molec. Cryst. Liq. Cryst. 8, 215–217 (1969)
Flory, P.J.: On the morphology of a crystalline state in polymers. J. Amer. Chem. Soc. 84, 2857–2867 (1962)
Frey-Wyssling, A.: Submicroscopic morphology of protoplasm. Amsterdam: Elsevier 1953
Gennes, P.J. de: The physics of liquid crystals. Oxford: Clarendon Press 1974
Giesbrecht, P.: Über das “Supercoiling” System der Chromosomen von Bacterien und Flagellaten und seine Beziehungen zu Nucleolus und Kerngrundsubstanz. Zbl. Bakt. I. Abt. Orig. 183, 1–44 (1961)
Giesbrecht, P.: Über das Ordnungsprinzip in den Chromosomen von Dinoflagellaten und Bacterien. Zbl. Bakt., I. Abt. Orig. 196, 516–519 (1965)
Grassé, P.P., Hollande, A., Cachon, J., Cachon-Enjumet, M.: Nouvelle interprétation du chromosome de certains Péridiniens. C.R. Acad. Sci. (Paris) 260, 1743–1747 (1965a)
Grassé, P.P., Hollande, A., Cachon, J., Cachon-Enjumet, M.: Interpretation de quelques aspects infrastructuraux des chromosomes de Péridininens en division. C.R. Acad. Sci. (Paris) 260, 6975–6977 (1965b)
Grell, K.G., Schwalbach, G.: Elektronenmikroskopische Untersuchungen an den Chromosomen der Dinoflagellaten. Chromosoma (Berl.) 17, 230–245 (1965)
Grund, S.: Hochgeordnete Feinstruktur des Chromosoms in Escherichia coli. Zbl. Med. Vet. B 21, 73–92 (1974)
Haapala, O.K., Soyer, M.O.: Structure of Dinoflagellate Chromosomes. Nature (Lond.) New Biol. 244, 195–197 (1973)
Haller, G. de, Kellenberger, E., Rouiller, C.: Etude au microcope electronique des plasmas contenant de l'acide desoxyribonucleique. J. de Microscopie 3, 627–643 (1964)
Himes, M., Beam, C.A.: Genetic analysis in the Dinoflagellate Crypthecodinium (Gyrodinium) cohnii: Evidence for unusual meiosis. Proc. nat. Acad. Sci. (Wash.) 72, 4546–4549 (1975)
Kowallik, K.V.: The use of proteases for improved presentation of DNA in chromosomes and chloroplasts of Prorocentrum micans. Arch. Mikrobiol. 80, 252–261 (1971)
Kubai, D.F., Ris, H.: Division in the Dinoflagellate Gyrodinium cohnii Sc., A New type of nuclear reproduction. J. Cell Biol. 40, 508–528 (1969)
Lerman, L.S.: Chromosomal analogues: Long-range order in condensed DNA. Cold Spr. Harb. Symp. quant. Biol. 38, 59–73 (1973)
Livolant, F., Giraud, M.M., Bouligand, Y.: A goniometric effect observed in sections of twisted fibrous materials. Biologie Cellulaire 31, 159–168 (1978)
Loeblich III, A.R.: Dinoflagellate genetics and DNA characterization. Stadler Symp. 8, 111–128 (1976)
Luzzati, V.: The structure of DNA as determined by X-Ray scattering techniques. Prog. Nucl. Acid. Res. 1, 347–368 (1963)
Mandelkern, L.: Crystallization in polymers, pp. 301–305, New York-San Francisco-Toronto-London: McGraw-Hill 1964
Matthys, E., Puiseux-Dao, S.: Les effets du bromure d'éthidium sur les ultrastructures des mitochondries et des plastes chez l'Amphidinium carteri. C.R. Acad. Sci. (Paris) 267, 2123–2125 (1968)
Monneron, A., Bernhard, W.: Fine structural organisation of the interphase nucleus in some mammalian cells. J. Ultrastruct. Res. 27, 266–288 (1969)
Oakley, B.R., Dodge, J.D.: Kinetochores associated with the nuclear envelope in the mitosis of a dinoflagellate. J. Cell Biol. 63, 322–325 (1974)
Provasoli, L.: Growing marine seaweeds. Proc. 4th Intern. Seaweed Symp. (Davy de Virville, A. and J. Feldman, eds.) Oxford-London-New York-Paris: Pergamon Press 1964
Reynolds, E.S.: The use of lead citrate at high pH as an electron opaze stain in electron microscopy. J. Cell Biol. 17, 208–211 (1963)
Ris, H.: Interpretation of ultrastructure in the Cell nucleus. In: The interpretation of ultrastructure (R.J.C. Harris, ed.), pp. 69–88. New York: Academic Press 1962
Ris, H., Kubai, D.F.: An unusual mitotic mechanism in the parasitic protozoan Syndinium sp. J. Cell Biol. 60, 702–720 (1974)
Rizzo, P.J., Nooden, L.D.: Isolation and Chemical composition of Dinoflagellate nuclei. J. Protozool. 20, 666–672 (1973)
Roberts, T.M., Lauer, G.D., Klotz, L.C.: Physical studies on DNA from “primitive” eucaryotes. Critical Rev. Biochem. 3, 349–449 (1976)
Roberts, T.M., Tuttle, R.C., Allen, J.R., Loeblich III, A.R., Klotz, L.C.: New genetic and physiological data on structure of Dinoflagellate chromosomes. Nature (Lond.) 248, 446–447 (1974)
Robinson, C.: Liquid crystalline structure in polypeptide solutions. Tetrahedron 13, 219–234 (1961)
Rouvière-Yaniv, J., Gros, F.: Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc. nat. Acad. Sci. (Wash.) 72, 3428–3442 (1975)
Rudall, K.M.: Protein ribbons and sheets. Lectures Scient. Basis Medic. 5, 217–230 (1955)
Ryter, A., Chang, A.: Localization of transcribing genes in the Bacterial cell by means of high voltage autoradiography. J. molec. Biol. 98, 797–810 (1975)
Sipski, M.L., Wagner, T.E.: The total structure and organisation of chromosomal fibers in Eutherian sperm nuclei. Biol. of Reproduction 16, 428–440 (1977)
Soyer, M.O.: Rapports existant entre chromosomes et membrane nucléaire chez un Dinoflagellé parasite du genre Blastodinium Chatton. C.R. Acad. Sci. (Paris) 268, 2082–2084 (1969)
Soyer, M.O.: Observations ultrastructurales sur la condensation sporogénétique des chromosomes chez Noctiluca miliaris. C.R. Acad. Sci. (Paris) 271, 1003–1006 (1970)
Soyer, M.O.: Structure du noyau de Blastodinium (Dinoflagellés parasites). Division et condensation chromatique. Chromosome (Berl.) 33, 70–114 (1971)
Soyer, M.O.: Les ultrastructures nucléaires de la Noctiluque (Dinoflagellé libre) au cours de la sporogénèse. Chromosoma (Berl.) 39, 419–441 (1972)
Soyer, M.O.: Étude ultrastructurale de Syndinium sp. Chatton, parasite coelomique de Copépodes pélagiques. Vie et Millieu 24, 191–212 (1974)
Soyer, M.O., Haapala, O.K.: Filaments extrachromosomiques: variations et relations avec l'enveloppe nucléaire pendant la division chez les Dinoflagellés. J. de Microscopie 18, 267–270 (1973)
Soyer, M.O., Haapala, O.K.: Electron microscopy of RNA in Dinoflagellate chromosomes. Histochemie 42, 239–246 (1974)
Soyer, M.O., Haapala, O.K.: Structural changes of Dinoflagellate chromosomes by pronase and ribonuclease. Chromosoma (Berl.) 47, 179–192 (1974)
Spencer, M.: X-ray diffraction studies of the secondary structure of RNA. Cold Spr. Harb. Symp. quant. Biol. 28, 77–82 (1963)
Spencer, M., Fuller, W., Wilkins, M.H.F., Brown, G.L.: Determination of the helical configuration of ribonucleic acid molecules by X-ray diffraction study of crystalline amino acid-transfer ribonucleic acid. Nature (Lond.) 194, 1014–1020 (1962)
Spencer, M., Poole, F.: On the origin of crystallizable RNA from yeast. J. molec. Biol. 11, 314–326 (1965)
Stosch, H.A.: Zum Problem der sexuellen Fortpflanzung in der Peridineen-Gattung Ceratium. Helgoländer Wiss. Meeresunters. 10, 140–155 (1964)
Tuttle, R.C., Loeblich III, A.R.: N-Methyl-N′-nitro-N-nitrosoguanidine and UV induced mutants of the Dinoflagellate Crypthecodinium cohnii. J. Protozool. 24, 313–316 (1977)
Worcel, A., Burgi, E.: On the structure of the folded chromosome of Escherichia coli. J. molec. Biol. 71, 127–147 (1972)
Zingmark, R.G.: Ultrastructural studies on two kinds of mesokaryotic nuclei. Amer. J. Bot. 57, 586–592 (1970)
Zubai, G., Watson, M.R.: The absence of histone in the Bacterium Escherichia coli. I Preparation and analysis of nucleoprotein extract. J. biol. biochem. Cytol. 5, 51–54 (1959)
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Livolant, F., Bouligand, Y. New observations on the twisted arrangement of Dinoflagellate chromosomes. Chromosoma 68, 21–44 (1978). https://doi.org/10.1007/BF00330370
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DOI: https://doi.org/10.1007/BF00330370