Summary
The nucleolus organizer (NO) of the D. melanogaster X chromosome is composed of ribosomal repeat units which contain two types (I and II) of non-rDNA insertions (In+) and repeats with no insertions (In-). Evidence from other laboratories indicate random interspersion of all types of repeat units within the X NO. An EcoRI and BamHI examination of rDNA from two bobbed mutants, bb 2rl and mal 12 demonstrates segregation of the major type I repeat units. The 46 rDNA repeats of the bb 2rl NO contain no detectable major type I repeats whereas the majority of the 68 rDNA mal 12 repeats are major type I and tandemly linked. This observation suggests that gross deletions of rDNA can result in nucleolus organizer regions with predominantly one type of repeat unit. Additivity tests demonstrate that the 46 ribosomal repeats of the bb 2rl chromosome revert the phenotype of other bobbed NOs, but the 68 mal 12 ribosomal repeats show no or slight additivity. This is in agreement with the observation that In+ repeats do not significantly contribute to functional rRNA. A Southern blot analysis using BamHI which cuts only in type I insertions demonstrates that the majority of major type I In+ repeating units exist in tandem linkage group(s) within the X NO.
Similar content being viewed by others
References
Beckingham K (1981) The ribosomal DNA of Calliphora erythrocephala: The cistron classes of total genomic DNA. J Mol Biol 149:141–169
Endow SA, Glover DM (1979) Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17:597–605
Franz G, Kunz W (1981) Intervening sequences in ribosomal rRNA genes and bobbed phenotype in Drosophila hydei. Nature 292:638–640
Gandhi VV, Sharp ZD, Procunier JD (1982) Analysis of Y chromosome nucleolar organizer mutants in Drosophila melanogaster. Biochem Biophys Res Commun 104:778–784
Glatzer KH (1979) Lengths of transcribed rDNA repeating units in spermatocytes of Drosophila hydei: Only genes without an intervening sequence are expressed. Chromosoma 75:161–175
Glover DM, Hogness DS (1977) A novel arrangement of the 18S and 28S sequences in a repeating unit of Drosophila melanogaster. Cell 10:167–176
Graziani F, Vicari L, Boncinelli E, Malva C, Manzi A, Mariani C (1981) Selective replication of ribosomal DNA repeats after loss of the abnormal oocyte phenotype in Drosophila melanogaster. Proc Natl Acad Sci USA 78:7662–7664
Indik ZK, Tartof KD (1980) Long spacers among ribosomal genes of Drosophila melanogaster. Nature 284:477–479
Kidd SJ, Glover DM (1980) A DNA segment from D. melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell 19:103–119
Kidd AJ, Glover DM (1981) Drosophila melanogaster ribosomal DNA containing type II insertions is variably transcribed in different strains and tissues. J Mol Biol 151:645–662
Korhorn BD, Rae PM (1982) Accurate transcription of truncated ribosomal DNA templates in a Drosophila cell-free system. Proc Natl Acad Sci USA 79:1501–1505
Laskey RA, Mills RD (1975) Quantitative film detection of 3H and 14C in polycrylamide gels by fluorography. Eur J Biochem 56:335–341
Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst Washington Publ 627
Long EO, Collins M, Kiefer BI, Dawid IB (1981) Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster. Mol Gen Genet 182:377–384
Long E, Dawid IB (1979) Expression of ribosomal DNA insertion in Drosophila melanogaster. Cell 18:1185–1196
Long EO, Rebbert ML, Dawid IB (1981) Nucleotide sequences of the initiation site for ribosomal RNA transcription in Drosophila melanogaster: Comparison of genes with and without insertions. Proc Natl Acad Sci USA 78:1513–1517
Peacock WJ, Appels R, Endow S, Glover D (1981) Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res Camb 37:209–214
Pellegrini M, Manning J, Davidson N (1977) Sequence arrangement of the rDNA of Drosophila melanogaster. Cell 10:213–224
Procunier JD, Williamson JH (1974) Temperature-sensitive bobbed mutants in Drosophila melanogaster. Dev Biol 39:198–209
Procunier JD, Tartof KD (1978) A genetic locus having trans and continguous cis functions that control the disproportionate replication of ribosomal RNA genes in Drosophila melanogaster. Genetics 88:67–79
Renkawitz-Pohl R, Glatzer KH, Kunz W (1980) Characterization of cloned ribosomal DNA from Drosophila hydei. Nucl Acids Res 98:4513–4611
Renkawitz-Pohl R, Glatzer KH, Kunz W (1981) Ribosomal RNA genes with an intervening sequence are clustered within the X chromosomal ribosomal DNA of Drosophila hydei. J Mol Biol 148:95–101
Ritossa FM, Atwood KC, Spiegelman S (1966) A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of “ribosomal” DNA. Genetics 54:819–834
Roiha H, Glover DM (1980) Characterization of complete type II insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. J Mol Biol 140:341–355
Roiha H, Glover DM (1981) Duplicated rDNA sequences of variable lengths flanking the short type I insertions in the rDNA of Drosophila melanogaster. Nucl Acids Res 9:5521–5532
Roiha H, Miller JR, Woods LC, Glover DM (1981) Arrangements and rearrangements of sequences flanking the two type of rDNA insertions in D. melanogaster. Nature 290:749–753
Schalet A (1969) Exchanges at the bobbed locus of Drosophila melanogaster. Genetics 63:133–153
Shermoen AW, Kiefer BI (1975) Regulation in rDNA-deficient Drosophila melanogaster. Cell 4:275–280
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517
Tartof K (1973) Regulation of ribosomal RNA gene multiplicity in Drosophila melanogaster. Genetics 73:57–51
Tartof K (1974) Unequal mitotic sister chromatid exchange as the mechanism of ribosomal RNA gene magnification. Proc Natl Acad Sci USA 71:1272–1276
Tartof KD, Dawid IB (1976) Similarities and differences in the structure of X and Y chromosome rRNA genes of Drosophila. Nature 263:27–30
Wahl GM, Stern M, Stark GR (1979) Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethylpaper and rapid hybridization by using dextran sulfate. Proc Nat Acad Sci USA 76:3683–3687
Wellauer PK, Dawid IB (1977) The structural organization of rDNA in D. melanogaster. Cell 10:193–212
Wellauer PK, Dawid IB, Tartof KD (1978) X and Y chromosomal ribosomal DNA of Drosophila: Comparison of spacers and insertions. Cell 14:269–278
White RL, Hogness DS (1977) R Loop mapping of the 18S and 28S sequences in the long and short repeating units of Drosophila melanogaster rDNA. Cell 10:177–192
Author information
Authors and Affiliations
Additional information
Communicated by K. Illmensee
Rights and permissions
About this article
Cite this article
Sharp, Z.D., Gandhi, V.V. & Procunier, J.D. X chromosome nucleolus organizer mutants which alter major type I repeat multiplicity in Drosophila melanogaster . Mol Gen Genet 190, 438–443 (1983). https://doi.org/10.1007/BF00331074
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00331074