Summary
We have shown earlier that interrupted rRNA genes in Drosophila melanogaster do not contribute significantly to rRNA production by a splicing mechanism (Long and Dawid 1979). In the work reported here the expression of interrupted rRNA genes was tested in several stocks that carry bobbed mutations, i.e., have partial deletions of their rRNA gene clusters. Transcripts of the major 5 kb type 1 insertion are very rare in bobbed flies as they are in the wild type, occurring at a concentration in embryos of less than one copy per nucleus. Transcripts of short type 1 insertions are more abundant in certain bobbed stocks, especially those carrying the car bb chromosome. However, other severely bobbed flies have no increase in these insertion transcripts over the low wild-type levels. Type 2 insertions are transcribed into very rare RNA molecules in the wild type and in the bobbed genotypes that were studied. From these results we conclude that interrupted rRNA genes are not expressed through a splicing mechanism into mature rRNA in mutant or wild-type flies. Since even severely bobbed flies fail to utilize their interrupted rRNA genes, we suggest that these genes cannot be transcribed productively in D. melanogaster.
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References
Barnett T, Rae PMM (1979) A 9.6 kb intervening sequence in D. virilis rDNA and sequence homology in rDNA interruptions of diverse species of Drosophila and other diptera. Cell 16:763–775
Beckingham K, White R (1980) The ribosomal DNA of Calliphora erythrocephala; an analysis of hybrid plasmids containing ribosomal DNA. J Mol Biol 137:349–373
Chooi WY (1979) The occurence of long transcription units among the X and Y ribosomal genes of Drosophila melanogaster: transcription of insertion sequences. Chromosoma 74:57–74
Clark SH, Kiefer BI (1977) Genetic modulation of RNA metabolism in Drosophila II. Coordinate rate change in 4S, 5S and poly(A)-associated RNA synthesis. Genetics 86:801–811
Clark SH, Strausbaugh LD, Kiefer BI (1977) Genetic modulation of RNA metabolism in Drosophila I. Increased rate of ribosomal RNA synthesis. Genetics 86:789–800
Dawid IB, Botchan P (1977) Sequences homologous to ribosomal insertions occur in the Drosophila genome outside the nucleolus organizer. Proc Natl Acad Sci USA 74:4233–4237
Dawid IB, Lauth M, Wellauer PK (1980) Repetitive DNA elements related to the ribosomal insertion of Drosophila melanogaster. In: Scott WR, Werner R, Joseph DR (eds) Mobilization and reassembly of genetic information, Miami Winter Symposium, vol 17, Academic Press, New York, pp 217–234
Dawid IB, Wellauer PK (1978) Ribosomal DNA and related sequences in Drosophila melanogaster. Cold Spring Harbor Symp Quant Biol 42:1185–1194
Dawid IB, Wellauer PK, Long EO (1978) Ribosomal DNA in Drosophila melanogaster. I. Isolation and characterization of cloned fragments. J Mol Biol 126:749–768
Endow SA, Glover DM (1979) Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell 17:597–605
Glätzer 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 rDNA. Cell 10:167–176
Graziani F, Gargano S (1976) Ribosomal DNA transcription products during the first steps of magnification in Drosophila melanogaster. J Mol Biol 100:59–71
Hennig W, Meer B (1971) Reduced polyteny of ribosomal RNA cistrons in giant chromosomes of Drosophia hydei. Nature 233:70–72
Jacobs-Lorena M (1980) Dosage of 5S and ribosomal genes during oogenesis of Drosophila melanogaster. Dev Biol 80:134–145
Jolly DJ, Thomas CA Jr (1980) Nuclear transcripts from Drosophila melanogaster ribosomal RNA genes containing introns. Nucleic Acids Res 8:67–84
Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster Carnegie Inst. Washington Publ. No. 627
Long EO, Dawid IB (1979) Expression of ribosomal DNA insertions in Drosophila melanogaster. Cell 18:1185–1196
Long EO, Dawid IB (1980a) Repeated genes in eukaryotes. Annu Rev Biochem 49:727–764
Long EO, Dawid IB (1980b) Alternative pathways in the processing of ribosomal RNA precursor in Drosophila melanogaster. J Mol Biol 138:873–878
Long EO, Rebbert ML, Dawid IB (1980) Structure and expression of ribosomal RNA genes of Drosophila melanogaster interrupted by type 2 insertions. Cold Spring Harbor Symp Quant Biol 45 (in press)
Long EO, Rebbert ML, Dawid IB (1981) The nucleotide sequence 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
McKnight SL, Miller OL Jr (1976) Ultrastructural patterns of RNA synthesis during embryogenesis of Drosophila melanogaster. Cell 8:305–319
Mermod JJ, Jacobs-Lorena M, Crippa M (1977) Changes in rate of RNA synthesis and ribosomal gene number during oogenesis of Drosophila melanogaster. Dev Biol 57:393–402
Meyer GF, Hennig W (1974) The nucleolus in primary spermatocytes of Drosophila hydel. Chromosoma (Berl) 46:121–144
Pellegrini M, Manning J, Davidson N (1977) Sequence arrangement of the rDNA of Drosophila melanogaster. Cell 10:213–224
Renkawitz-Pohl R, Glätzer KH, Kunz W (1980) Characterization of cloned ribosomal DNA from Drosophila hydei. Nucl Acids Res 8:4593–4611
Ritossa F (1976) The Bobbed Locus. In: Ashburner M, Novitski E (eds) The genetics and biology of Drosophila, vol. 1a. Academic Press, New York
Roiha H, Glover DM (1980) Characterization of complete type 2 insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. J Mol Biol 140:341–355
Shermoen AW, Kiefer BI (1975) Regulation in rDNA-deficient Drosophila melanogaster. Cell 4:275–280
Simoncsits A, Brownlee GG, Brown RS, Rubin JR, Guilley H (1977) New rapid gel sequencing method for RNA. Nature 269:833–836
Spear BB (1974) The genes for ribosomal RNA in diploid and polytene chromosomes of Drosophila melanogaster. Chromosoma 48:159–179
Spear BB, Gall JG (1973) Independent control of ribosomal gene replication in polytene chromosomes of Drosophila melanogaster. Proc Natl Acad Sci USA 70:1359–1363
Strausbaugh LD (1977) PhD Thesis, Wesleyan University, Middletown, Conn.
Tartof KD (1975) Redundant Genes. Ann Rev Genet 9:355–385
Weinmann R (1972) Regulation of ribosomal RNA and 5S RNA synthesis in Drosophila melanogaster: I. Bobbed mutants. Genetics 72:267–276
Wellauer PK, Dawid IB (1977) The structural organization of ribosomal DNA in Drosophila melanogaster. Cell 10:103–212
Wellauer PK, Dawid IB (1978) Ribosomal DNA in Drosophila melanogaster. II. Heteroduplex mapping of cloned and uncloned rDNA. J Mol Biol 126:769–782
Wellauer PK, Dawid IB, Tartof KD (1978) X and Y chromosomal ribosomal DNA of Drosophila: comparison of spacers and insertions. Cell 14:269–278
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Long, E.O., Collins, M., Kiefer, B.I. et al. Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster . Molec. Gen. Genet. 182, 377–384 (1981). https://doi.org/10.1007/BF00293925
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DOI: https://doi.org/10.1007/BF00293925