Abstract
Using in situ nucleic acid hybridizations, the genes that code for 28, 18 and 5S rRNA have been localized in the polytene chromosomes of Drosophila tumiditarsus. The 5S genes are found at a single site near the centromere of the second chromosome, whereas the 28 and 18S genes are found at the nucleolar organizer region of the dot chromosome. The dot chromosome has been previously described as α-heterochromatic. However, our cytochemical and autoradiographic results do not support such a conclusion. The autoradiographic results reveal that the dot chromosome is transcriptionally active and is not late-replicating, as is expected of α-heterochromatin. Further, the dot chromosomes possess none of the usual staining characteristics of heterochromatin except for its lack of polytene bands. Using rRNA-DNA filter hybridizations, we find that the rDNA of D. tumiditarsus salivary glands is under-replicated. This is the first species of Drosophila where the rDNA in not found on the sex chromosomes, and is the first report of an under-replicated autosomal locus which is not located in heterochromatic blocks.
Similar content being viewed by others
References
Alonso, C., Berendes, H.D.: The location of 5S (ribosomal) RNA genes in Drosophila hydei. Chromosoma (Berl.) 51, 347–356 (1975)
Barr, H.J.: Comparative morphology of nucleolar DNA in Drosophila. II. Drosophila fulvimaculoides and Drosophila tumiditarsus. J. Morph. 134, 243–258 (1971)
Bäumlein, H., Wobus, U.: Chromosomal localization of ribosomal 5S RNA genes in Chironomus thummi by in situ hybridization of iodinated 5S RNA. Chromosoma (Berl.) 57, 199–204 (1976)
Berendes, H.D.: Differential replication of male and female X-chromosomes in Drosophila. Chromosoma (Berl.) 20, 32–43 (1966)
Bicudo, H.E.-M.C., Richardson, R.H.: Gene regulation in Drosophila mulleri and D. arizonensis and their hybrids: The nucleolar organizer. Proc. nat. Acad. Sci. (Wash.) 74, 3498–3502 (1977)
Cohen, M.: Ectopic pairing and evolution of 5S ribosomal RNA genes in the chromosomes of Drosophila funebris. Chromosoma (Berl.) 55, 349–357 (1976)
Cummings, M.R., King, R.C.: The cytology of the vitellogenic stages of oogenesis in Drosophila melanogaster. I. General staging characteristics. J. Morph. 128, 427–442 (1969)
Dart, L.H., Turner, T.R.: Fluorescent microscopy of exfoliative cytology. Lab. Invest. 8, 1513–1522 (1959)
Eckhardt, R.A.: Cytological localizations of repeated DNAs. In: Handbook of genetics (R.C. King, ed.), vol. 5, pp. 31–53. New York: Plenum Press 1976
Endow, S.A., Gall, J.G.: Differential replication of satellite DNA in polyploid tissues of Drosophila virilis. Chromosoma (Berl.) 50, 175–192 (1975)
Endow, S.A., Glover, D.: Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17, 597–605 (1979)
Gambarini, A.G., Lara, J.S.: Underreplication of ribosomal cistrons in polytene chromosomes of Rhynchosciara. J. Cell Biol. 63, 215–222 (1974)
Gillespie, D., Spiegelman, S.: A quantitative assay for DNA-RNA hybrids with DNA immobilized on a membrane. J. molec. Biol. 12, 829–842 (1965)
Hägele, K., Kalisch, W.E.: Initial phases of DNA synthesis in Drosophila melanogaster. I. Differential participation in replication of the X chromosome in males and females. Chromosoma (Berl.) 47, 403–413 (1974)
Hall, T., Cummings, M.: In vitro synthesis and processing of ribosomal RNA in the housefly ovary. Develop. Biol. 46, 233–242 (1975)
Hennig, W., Meer, B.: Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophila hydei. Nature (Lond.) New Biol. 233, 70–72 (1971)
Hochman, B.: The fourth chromosome of Drosophila melanogaster. In: Genetics and biology of Drosophila (M. Ashburner and E. Novitski. eds.), vol. 1 b, pp. 903–928. New York: Academic Press 1976
Hollenberg, C.D.: Proportionate representation of rDNA and Balbiani ring DNA in polytene chromosomes of Chironomus tentans. Chromosoma (Berl.) 57, 185–197 (1976)
Holmquist, G., Steffensen, D.M.: Evidence for a specific three-dimensional arrangement of polytene chromosomes by nuclear membrane attachments. J. Cell Biol. 59, 147a (1973)
Hsiang, W.: The distribution of heterochromatin in Drosophila tumiditarsus. Cytologia (Tokyo) 14, 149–152 (1949)
Kaufmann, B.P., Gay, H.: The capacity of the fourth chromosome of Drosophila melanogaster to establish end to end contacts with the other chromosomes in salivary gland cells. Chromosoma (Berl.) 26, 395–409 (1969)
Krivshenko, J.: New evidence for the homology of the short euchromatic elements of the X and Y chromosomes of Drosophila busckii with the microchromosome of Drosophila melanogaster. Genetics 44, 1027–1040 (1959)
Lakhotia, S.C.: Autoradiographic studies on polytene nuclei of Drosophila melanogaster III. Localization of non-replicating chromatin in the chromocenter heterochromatin. Chromosoma (Berl.) 46, 145–159 (1974)
Lakhotia, S.C., Jacob, J.: EM autoradiographic studies on polytene nuclei of Drosophila melanogaster II. Organization and transciptive activity of the chromocenter. Exp. Cell Res. 86, 253–263 (1974)
Lakhotia, S.C., Mukherjee, A.S.: Chromosomal basis of dosage compensation in Drosophila. III. Early completion of replication by the polytene X chromosome in males. J. Cell Biol. 47, 18–33 (1970)
Lima-de-Faria, A.: The specific location of ribosomal genes in the eucaryotic chromosome. In: Modern aspects of cytogenetics: Constitutive heterochromatin in man. Symp. Med. Hoechst, pp. 39–44. Stuttgart and New York: Schattauer 1973
Meer, B.: Anomalous development and differential DNA replication in the X-chromosome of a Drosophila hybrid. Chromosoma (Berl.) 57, 235–260 (1976)
Mohan, J.: Multiplicity of ribosomal RNA genes in Drosophila melanogaster during growth and development. Dros. Inf. Serv. 52, 132 (1977)
Nash, D., Vyse, E.R.: On the polytene morphology of a Drosophila melanogaster chromosomal inversion including the nucleolus organizer. Canad. J. Genet. Cytol. 19, 637–644 (1977)
Pardue, M.L., Gerbi, S.A., Echkardt, R.A., Gall, J.G.: Cytological localization of DNA complementary to ribosomal RNA in polytene chromosomes of Diptera. Chromosoma (Berl.) 29, 268–290 (1970)
Plaut, W.: On ordered DNA replication in polytene chromosomes. Genetics, Suppl. 61, 239–244 (1969)
Prensky, W.: The radioiodination of RNA and DNA to high specific activities. Methods in cell biol. 13, 121–152 (1975)
Renkawitz, R., Kunz, W.: Independent replication of the ribosomal RNA genes in the polytrophic meroistic ovaries of Calliphora erythrocephala, Drosophila hydei and Sarcophaga barbata. Chromosoma (Berl.) 53, 131–140 (1975)
Rudkin, G.T.: Non-replicating DNA in Drosophila. Genetics, Suppl. 61, 227–238 (1969)
Sande, J.H., van de, Lin, C.C., Jorgenson, K.F.: Reverse banding on chromosomes produced by a guanosine-cytosine specific DNA binding antibiotic: Olivomycin. Science 195, 400–402 (1977)
Sandler, L.M., Novitski, E.: Evidence for genetic homology between chromosomes 1 and 4 in Drosophila melanogaster, with a proposed explanation for the crowding effect in triploids. Genetics 41, 189–193 (1956)
Shermoen, A.W., Kiefer, B.: Regulation in rDNA deficient Drosophila melanogaster. Cell 4, 275–280 (1975)
Sinibaldi, R.M.: Localization and characterization of rDNA in Drosophila tumiditarsus, Ph.D. thesis, University of Illinois, Chicago. (1978)
Sinibaldi, R.M., M. Cummings: Localization of genes for 28S, 18S and 5S rRNA in Drosophila tumiditarsus. J. Cell Biol. 75, 128a (1977)
Sinibaldi, R.M., Cummings. M.: Characterization of the dot chromosome in Drosophila tumiditarsus. J. Cell Biol. 79, 128a (1978)
Sinibaldi, R.M., Grilly, M.E., Barr, H.J.: Characterization of the toromeric structure in Drosophilia lummei. Chromosoma (Berl.) 58, 63–71 (1976)
Sokoloff, S.: Replication of polytene chromosomes in the dipteran Phryne, Ph.D. thesis, Fachbereich Biologie, Universität Tübingen (1977)
Spear, B.: The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma (Berl.) 48, 159–179 (1974)
Spear, B., Gall, J.G.: Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc. nat. Acad. Sci. (Wash.) 70, 1359–1363 (1973)
Spradling, A., Penman, S., Pardue, M.L.: Analysis of Drosophila mRNA in in situ hybridization: Sequences transcribed in normal and heat shocked cultured cells. Cell 4, 395–404 (1975)
Szabo, P.: The localization of genes; Studies with in situ hybridization. Ph.D. thesis, University of Illinois, Urbana. (1974)
Szabo, P., Elder, R., Steffensen, D.M., Uhlenbeck, O.C.: Quantitative in situ hybridization of ribosomal RNA species to polytene chromosomes of Drosophila melanogaster. J. molec. Biol. 115, 539–563 (1977)
Tartof, K.D.: Redundant genes. Ann. Rev. Genet. 9, 355–385 (1975)
Wen, W., Leon, P.E., Hague, D.R.: Multiple gene for 5S and 18 28S RNA on chromosomes of Glypotendiples barbipes (Staeger). J. Cell Biol. 62, 132–144 (1974)
Wieslander, L., Lambert, B., Egyházi, E.: Localization of the 5S RNA genes in Chironomus tentans. Chromosoma (Berl.) 51, 49–56 (1975)
Wimber, D.E., Duffey, P.A., Steffensen, D.M., Prensky, W.: Localization of the 5S RNA genes in Zea mays by RNA-DNA hybridization in situ. Chromosoma (Berl.) 47, 353–359 (1974)
Wimber, D.E., Wimber, D.R.: Sites of the 5S ribosomal gene in Drosophila. I. The multiple clusters in the virilis group. Genetics 86, 133–148 (1977)
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sinibaldi, R.M., Cummings, M.R. Localization and characterization of rDNA in Drosophila tumiditarsus . Chromosoma 81, 655–671 (1981). https://doi.org/10.1007/BF00329578
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00329578