Abstract
In Drosophila melanogaster it is now documented that the different satellite DNA sequences make up the majority of the centromeric heterochromatin of all chromosomes. The most popular hypothesis on this class of DNA is that satellite DNA itself is important to the pairing processes of chromosomes. Evidence in support of such a hypothesis is, however, circumstantial. This hypothesis has been evaluated by direct cytological examination of the meiotic behaviour of heterochromatically and/or euchromatically rearranged autosomes in the male. It was found that neither substantial deletions nor rearrangements of the autosomal heterochromatin cause any disruption of meiotic pairing. Autosomal pairing depends on homologs retaining sufficient euchromatic homology. This is the first clear demonstration that the highly repeated satellite DNA sequences in the heterochromatin of the second, third and fourth chromosomes are not important in meiotic pairing, but rather that some euchromatic homology in the autosomes is essential to ensure a regular meiotic process. These results on the autosomes, when taken in conjunction with our previous studies on sex chromosome pairing, clearly indicate that satellite DNA is not crucial for male meiotic chromosome pairing of any member of the D. melanogaster genome.
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Árnason, Ú.: Comparative chromosome studies in Cetacea. Hereditas (Lund.) 77, 1–36 (1974)
Arrighi, F.E., Hsu, T.C., Pathak, S., Sawada, H.: The sex chromosomes of the Chinese hamster: constitutive heterochromatin deficient in repetitive DNA sequences. Cytogenet. Cell Genet. 13, 268–274 (1974)
Au, W., Feckheimer, N.S., Soukup, S.: Identification of the sex chromosomes in the bald eagle. Canad. J. Genet. Cytol. 17, 187–191 (1975)
Baker, B.S., Hall, J.C.: Meiotic mutants: Genetic control of meiotic recombination and chromosome segregation. In: The genetics and biology of Drosophila (M. Ashburner and E. Novitski, eds.), Vol. 1b, pp. 351–434. London: Academic Press 1976
Baverstock, P.R., Watts, C.H.S., Hogarth, J.T.: Heterochromatin variation in the Australian rodent Uromys caudimaculatus. Chromosoma (Berl.) 57, 397–403 (1976)
Baverstock, P.R., Watts, C.H.S., Hogarth, J.T.: Polymorphism of the X-chromosome, Y-chromosome and autosomes in the Australian hopping mice, Notomys alexis, N. cervinus and N. fuscus (Rodentia, Muridae). Chromosoma (Berl.) 61, 243–256 (1977)
Bianchi, N.O., Vidal-Rioja, L., Bianchi, M.S.: Constitutive heterochromatin G-bands and robertsonian rearrangements in the chromosomes of Akodon molinae (Rodentia: Cricetidae). Canad. J. Genet. Cytol. 15, 855–861 (1973)
Bickham, J.W., Baker, R.J.: Chromosome homology and evolution of Emydid turtles. Chromosoma (Berl.) 54, 201–219 (1976)
Blumenfeld, M.: The evolution of satellite DNA in Drosophila virilis. Cold Spring Harb. Symp. quant. Biol. 38, 423–427 (1973)
Blumenfeld, M., Forrest, H.S.: Differential under-replication of satellite DNAs during Drosophila development. Nature (Lond.) New Biology 239, 170–172 (1972)
Bowman, J.G., Rajhathy, T.: Fusion of chromocenters in premeiotic interphase of Secale cereale and its possible relationship to chromosome pairing. Canad. J. Genet. Cytol. 19, 313–321 (1977)
Brosseau, G.E., Lindsley, D.L.: A dominantly marked Y chromosome: YBs. Dros. Inf. Serv. 32, 116 (1958)
Brown, J.E., Jones, K.W.: Localization of satellite DNA in the microchromosomes of the Japanese quail by in situ hybridization. Chromosoma (Berl.) 38, 313–318 (1972)
Brutlag, D.L., Peacock, W.J.: Sequences of highly repeated DNA in Drosophila melanogaster. In: The eukaryote chromosome (W.J. Peacock and R.D. Brock, eds), pp. 35–45. Canberra: Australian National University Press 1975
Buckland, R.A., Fletcher, J.M., Chandley, A.C.: Characterization of the domestic horse (Equus caballus) karyotype using G-and C-banding techniques. Experientia (Basel) 32, 1146–1149 (1976)
Buckton, K.E., O'riordan, M.L., Jacobs, P.A., Robinson, J.A., Hill, R., Evans, H.J.: C-and Q-band polymorphism in the chromosomes of three human populations. Ann. Hum. Genet. 40, 99–112 (1976)
Cooper, K.W.: Meiotic conjunctive elements not involving chiasmata. Proc. Nat. Acad. Sci (Wash.) 52, 1248–1255 (1964)
Cooper, K.W.: Normal spermatogenesis in Drosophila. In: Biology of Drosophila (M. Demerec, ed.), pp. 1–61. New York: Hafner Pub. Comp. 1965
Dev, V.G., Miller, D.A., Miller, O.J.: Chromosome markers in Mus musculus: Strain differences in C-banding. Genetics 75, 663–670 (1973)
Dev, V.G., Miller, D.A., Tantravahi, R., Schreck, R.R., Roderick, T.H., Erlanger, B.F., Miller, O.J.: Chromosome markers in Mus musculus: Differences in C-banding between the subspecies M. m. musculus and M. m. molossinus. Chromosoma (Berl.) 53, 335–344 (1975)
Dobzhansky, T.: The decrease in crossing-ober observed in translocations and its probable explanation. Amer. Naturalist 65, 214–232 (1931)
Evans, H.J., Buckland, R.A., Sumner, A.T.: Chromosome homology and heterochromatin in Goat, Sheep and Ox studied by banding techniques. Chromosoma (Berl.) 42, 383–402 (1973)
Flamm, W.G.: Highly repetitive sequences of DNA in chromosomes. Int. Rev. Cytol. 32, 1–51 (1972)
Forejt, J.: Centromeric heterochromatin polymorphism in the house mouse. Chromosoma (Berl.) 43, 187–201 (1973)
Fredga, K., Mandahl, N.: Autosomal heterochromatin in some carnivores. In: Chromosome identification, pp. 104–117. New York and London: Academic Press 1973
Geraedts, J.P.M., Pearson, P.L., Van Der Ploeg, M., Vossepoel, A.M.: Polymorphisms for human chromosomes 1 and Y. Feulgen and UV DNA Measurements. Exp. Cell Res. 95, 9–14 (1975)
Gethmann, R.C.: Meiosis in male Drosophila melanogaster. II. Nonrandom segregation of compound-second chromosomes. Genetics 83, 743–751 (1976)
Grell, E.H.: Distributive pairing: Mechanism for segregation of compound autosomal chromosomes in oocytes of Drosophila melanogaster. Genetics 65, 65–74 (1970)
Hansen, K.M.: Heterochromatin (C-bands) in bovine chromosomes. Hereditas (Lund) 73, 65–70 (1973)
Hansmann, I.: Structural variability of human chromosome 9 in relation to its evolution. Hum. Genet. 31, 247–262 (1976)
Hilliker, A.J., Holm, D.G.: Genetic analysis of the proximal region of chromosome 2 of Drosophila melanogaster. I. Detachment products of compound autosomes. Genetics 81, 705–721 (1975)
Holm, D.G.: Compound autosomes. In: The genetics and biology of Drosophila (M. Ashburner and E. Novitski, eds.), Vol 1b,pp. 529–561. London: Academic Press 1976
Hsu, T.C., Cooper, J.E.K., Mace, M.L. Jr., Brinkley, B.R.: Arrangement of centromeres in mouse cells. Chromosoma (Berl.) 34, 73–87 (1971)
Imai, H.T., Crozier, R.H., Taylor, R.W.: Karyotype evolution in Australian Ants. Chromosoma (Berl.) 59, 341–393 (1977)
John, B.: Myths and mechanisms of meiosis. Chromosoma (Berl.) 54, 295–325 (1976)
John, B., King, M.: Heterochromatin variation in Cryptobothrus chrysophorus II. Patterns of C-banding. Chromosoma (Berl.) 65, 59–79 (1977)
John, B., Lewis, K.R.: The meiotic mechanism. In: Oxford Biology Readers (J.J. Head, ed.), 65, pp. 1–32. Oxford: Oxford University Press 1973
John, B., Miklos, G.L.G.: Functional aspects of satellite DNA and heterochromatin. Int. Rev. Cytol. 58 (in press, 1979)
Johnsen, R.C.: Cytogenetics of a univalent chromosome in Bs Drosophila melanogaster males. Canad. J. Genet. Cytol. 13, 81–89 (1971)
Jones, K.W., Corneo, G.: Location of satellite and homogeneous DNA sequences on human chromosomes. Nature (Lond.) New Biol. 233, 268–271 (1971)
Jones, K.W., Prosser, J., Corneo, G., Ginelli, E.: The chromosomal location of human satellite DNA III. Chromosoma (Berl.) 42, 445–451 (1973)
Jones, K.W., Purdom, I.F., Prosser, J., Corneo, G.: The chromosomal localization of human satellite I. Chromosoma (Berl.) 49, 161–171 (1974)
Kato, H., Tsuchiya, K., Yosida, T.H.: Constitutive heterochromatin of Indian muntjac chromosomes revealed by DNase treatment and a G-banding technique. Canad. J. Genet. Cytol. 16, 273–280 (1974)
Kurnit, D.M., Shafit, B.R., Maio, J.J.: Multiple satellite deoxyribonucleic acids in the Calf and their relation to the sex chromosomes. J. Mol. Biol. 81, 273–284 (1973)
Lindsley, D.L., Grell, E.H.: Genetic variations of Drosophila melanogaster. Carnegie Inst. Washington Publ. 627 (1968)
Lubs, H.A., Kimberling, W.J., Hecht, F., Patil, S.R., Brown, J., Gerald, P., Summitt, R.L.: Racial differences in the frequency of Q and C chromosomal heteromorphism. Nature (Lond.) 268, 631–633 (1977)
Lubs, H.A., Ruddle, F.H.: Chromosome polymorphism in American negro and white populations. Nature (Lond.) 233, 134–136 (1971)
Lütolf, H.U.: Meiotic segregation of compound-3 chromosomes in Drosophila. Genetica (Den Haag) 43, 431–442 (1972)
McKenzie, W.H., Lubs, H.A.: Human Q and C chromosomal variations: distribution and incidence. Cytogenet. Cell Genet. 14, 97–115 (1975)
Miklos, G.L.G., John, B.: Heterochromatin and satellite DNA in man: Properties and prospects. Amer. J. Hum. Gen. (in press 1979)
Mitchell, A.R., Seuanez, H.N., Lawrie, S.S., Martin, D.E., Gosden, J.R.: The location of DNA homologous to human satellite DNA in the chromosomes of chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla) and orangutan (Pongo pygmaeus). Chromosoma (Berl.) 61, 345–358 (1977)
Morgan, T.H., Schultz, J., Curry, V.: Investigations on the constitution of the germinal material in relation to heredity. Carnegie Inst, Washington Year Book 39, 251–255 (1939–1940)
Moses, M.J.: Synaptonemal complex karyotyping in spermatocytes of the Chinese Hamster. Chromosoma (Berl.) 60, 127–137 (1977)
Moses, M.J., Counce, S.J., Paulson, D.F.: Synaptonemal complex complement of man in spreads of spermatocytes, with details of the sex chromosome pair. Science 187, 363–365 (1975)
Moses, M.J., Russell, L.B., Cacheiro, N.L.A.: Mouse chromosome translocations: visualization and analysis by electron microscopy of the synaptonemal complex. Science 196, 892–894 (1977)
Muller, H.J., Pontecorvo, G.: Recombinants between Drosophila species the F1 hybrids of which are sterile. Nature (Lond.) 146, 199–200 (1940)
Muller, H.J., Pontecorvo, G.: Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27, 157 (1942)
Müntzing, A.: The meiotic pairing of iso-chromosomes in rye. Portug. Acta Biol., ser. A, R.B. Goldschmidt Volumen, 831–860 (1951)
Nankivell, R.N.: Karyotype differences in the crenaticeps group of Atractomorpha (Orthoptera, Acridoidea, Pyrgomorphidae). Chromosoma (Berl.) 56, 127–142 (1976)
Oshima, C.: Genetic studies on the hybrids of three subspecies of Drosophila virilis (II). Jap. J. Genet. 23, 96–103 (1948)
Oshima, C.: Genetic Studies on the hybrids of three species of Drosophila virilis III. Coordinating Commit. for Res. in Genetics 1, 99–107 (1950)
Oshima, C.: Factors involved in the evolution of animal populations. In: Ecology and evolution. The modern biology, Vol. 9, pp. 185–206. Iwanami Shoten, Tokyo 1966
Pardue, M.L., Gall, J.G.: Chromosomal localization of mouse satellite DNA. Science 168, 1356–1358 (1970)
Pathak, S., Wurster-Hill, D.H.: Distribution of constitutive heterochromatin in carnivores. Cytogenet. Cell Genet. 18, 245–254 (1977)
Peacock, W.J., Appels, R., Dunsmuir, P., Lohe, A.R., Gerlach, W.L.: Highly repeated DNA sequences: Chromosomal localization and evolutionary conservatism. In: International cell biology (ed. B.R. Brinkley and K.R. Porter), pp. 494–506. New York: Rockefeller Univ. Press 1977
Rasmussen, I.E.: New mutants. Dros. Inf. Serv. 34, 53 (1960)
Rasmussen, S.W.: Ultrastructural studies of spermatogenesis in Drosophila melanogaster Meigen. Z. Zellforsch. 140, 125–144 (1973)
Rhoades, M.M.: A new type of translocation in Drosophila melanogaster. Genetics 16, 490–504 (1931)
Rice, N.R., Straus, N.A.: Relatedness of mouse satellite deoxyribonucleic acid to deoxyribonucleic acid of various Mus species. Proc. Nat. Acad. Sci. (Wash.) 70, 3546–3550 (1973)
Sandler, L., Lindsley, D.L., Nicoletti, B., Trippa, G.: Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics 60, 525–558 (1968)
Schmid, W.: Heterochromatin in mammals. Arch. Julius Klaus Stift. Vererbungsforsch. 42, 1–60 (1967)
Schnedl, W., Czaker, R.: Centromeric heterochromatin and comparison of G-banding in cattle, goat, and sheep chromosomes (Bovidae). Cytogenet. Cell Genet. 13, 246–255 (1974)
Singh, L., Purdom, I.F., Jones, K.W.: The chromosomal localisation of satellite DNA in Ptyas mucosus (Ophidia, Colubridae). Chromosoma (Berl.) 57, 177–184 (1976a)
Singh, L., Purdom, I.F., Jones. K.W.: Satellite DNA and evolution of sex chromosomes. Chromosoma (Berl.) 59, 43–62 (1976b)
Singh, L., Ray-Chaudhuri, S.P.: Localization of C-band in the W sex chromosome of common Indian krait, Bungarus caeruleus Schneider. Nucleus (Calcutta) 18, 163–166 (1975)
Sinha, A.K., Kakati, S.: C and G-bands of the opossum chromosomes: Terminal sequences of DNA replication. Canad. J. Genet. Cytol. 18, 195–205 (1976)
Solari, A.J.: The behavior of the XY pair in mammals. Int. Rev. Cytol. 38, 273–317 (1974)
Solari, A.J., Ashley, T.: Ultrastructure and behaviour of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus). Chromosoma (Berl.) 62, 319–336 (1977)
Stefos, K., Arrighi, F.E.: Heterochromatic nature of W chromosome in birds. Exp. Cell Res. 68, 228–231 (1971)
Stefos, K., Arrighi, F.E.: Repetitive DNA of Gallus domesticus and its cytological locations. Exp. Cell Res. 83, 9–14 (1974)
Stern, C.: Zytologisch-genetische Untersuchungen als Beweise für die Morgansche Theorie des Faktorenaustauschs. Biol. Zbl. 51, 547–587 (1931)
Stone, W.: Linkage between the X and IV chromosomes in Drosophila melanogaster. Genetica ('s-Gravenhage) 16, 506–519 (1934)
Tettenborn, U., Gropp, A.: Meiotic nondisjunction in mice and mouse hybrids. Cytogenetics 9, 272–283 (1970)
Voiculescu, I., Vogel, W., Wolf, U.: Karyotyp und Heterochromatinmuster des rumänischen Hamsters (Mesocricetus newtoni). Chromosoma (Berl.) 39, 215–224 (1972)
Walker, P.M.B., Flamm, W.G., McLaren, A.: Highly repetitive DNA in rodents. In: Handbook of molecular cytology (A. Lima-de-Faria, ed.), pp. 52–66. Amsterdam-London: North-Holland Pub. Comp. 1969
Yamamoto, M., Miklos, G.L.G.: Genetic dissection of heterochromatin in Drosophila: The role of basal X heterochromatin in meiotic sex chromosome behaviour. Chromosoma (Berl.) 60, 283–296 (1977)
Yamamoto, M., Miklos, G.L.G.: Genetic studies on heterochromatin in Drosophila melanogaster and their implications for the functions of satellite DNA. Chromosoma (Berl.) 66, 71–98 (1978)
Yosida, T.H.: Diminution of heterochromatic C-bands in relation to the differentiation of Rattus species. Proc. Japan Acad. 51, 659–663 (1975)
Yosida, T.H., Sagai, T.: Variation of C-bands in the chromosomes of several subspecies of Rattus rattus. Chromosoma (Berl.) 50, 283–300 (1975)
Yunis, J.J., Yasmineh, W.G.: Model for mammalian constitutive heterochromatin. Advanc. Cell. molec. Biol. (E.J. DuPraw, ed.),Vol. 2, 1–46. London: Academic Press 1972
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Yamamoto, M. Cytological studies of heterochromatin function in the Drosophila melanogaster male: autosomal meiotic pairing. Chromosoma 72, 293–328 (1979). https://doi.org/10.1007/BF00331091
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DOI: https://doi.org/10.1007/BF00331091