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. 1984 Jul 11;12(13):5495–5513. doi: 10.1093/nar/12.13.5495

Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene.

P O O'Connell, M Rosbash
PMCID: PMC318935  PMID: 6087289

Abstract

In this communication, we describe several features of the D. melanogaster gene which codes for ribosomal protein 49 (rp49). Nucleotide sequence analysis in conjunction with primer extension and S1 nuclease protection experiments show that the structure of the rp49 gene consists of a 102 bp 5' exon, a single 59 bp intron, and a 420 bp 3' exon, encoding a total of 132 amino acids. The rp49 gene shares many features with other abundantly expressed Drosophila genes, including codon preference, which are discussed.

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  1. Bennetzen J. L., Hall B. D. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
  2. Benoist C., O'Hare K., Breathnach R., Chambon P. The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res. 1980 Jan 11;8(1):127–142. doi: 10.1093/nar/8.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  4. Bollen G. H., Cohen L. H., Mager W. H., Klaassen A. W., Planta R. J. Isolation of cloned ribosomal protein genes from the yeast Saccharomyces carlsbergensis. Gene. 1981 Sep;14(4):279–287. doi: 10.1016/0378-1119(81)90160-8. [DOI] [PubMed] [Google Scholar]
  5. Bozzoni I., Beccari E., Luo Z. X., Amaldi F. Xenopus laevis ribosomal protein genes: isolation of recombinant cDNA clones and study of the genomic organization. Nucleic Acids Res. 1981 Mar 11;9(5):1069–1086. doi: 10.1093/nar/9.5.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bozzoni I., Tognoni A., Pierandrei-Amaldi P., Beccari E., Buongiorno-Nardelli M., Amaldi F. Isolation and structural analysis of ribosomal protein genes in Xenopus laevis. Homology between sequences present in the gene and in several different messenger RNAs. J Mol Biol. 1982 Nov 5;161(3):353–371. doi: 10.1016/0022-2836(82)90244-3. [DOI] [PubMed] [Google Scholar]
  7. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  8. Busslinger M., Portmann R., Irminger J. C., Birnstiel M. L. Ubiquitous and gene-specific regulatory 5' sequences in a sea urchin histone DNA clone coding for histone protein variants. Nucleic Acids Res. 1980 Mar 11;8(5):957–977. doi: 10.1093/nar/8.5.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Corden J., Wasylyk B., Buchwalder A., Sassone-Corsi P., Kedinger C., Chambon P. Promoter sequences of eukaryotic protein-coding genes. Science. 1980 Sep 19;209(4463):1406–1414. doi: 10.1126/science.6251548. [DOI] [PubMed] [Google Scholar]
  10. D'Eustachio P., Meyuhas O., Ruddle F., Perry R. P. Chromosomal distribution of ribosomal protein genes in the mouse. Cell. 1981 May;24(2):307–312. doi: 10.1016/0092-8674(81)90320-2. [DOI] [PubMed] [Google Scholar]
  11. Fabijanski S., Pellegrini M. Isolation of a cloned DNA segment containing a ribosomal protein gene of Drosophila melanogaster. Gene. 1982 Jun;18(3):267–276. doi: 10.1016/0378-1119(82)90165-2. [DOI] [PubMed] [Google Scholar]
  12. Faliks D., Meyuhas O. Coordinate regulation of ribosomal protein mRNA level in regenerating rat liver. Study with the corresponding mouse cloned cDNAs. Nucleic Acids Res. 1982 Feb 11;10(3):789–801. doi: 10.1093/nar/10.3.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fitzgerald M., Shenk T. The sequence 5'-AAUAAA-3'forms parts of the recognition site for polyadenylation of late SV40 mRNAs. Cell. 1981 Apr;24(1):251–260. doi: 10.1016/0092-8674(81)90521-3. [DOI] [PubMed] [Google Scholar]
  14. Fried H. M., Pearson N. J., Kim C. H., Warner J. R. The genes for fifteen ribosomal proteins of Saccharomyces cerevisiae. J Biol Chem. 1981 Oct 10;256(19):10176–10183. [PubMed] [Google Scholar]
  15. Geyer P. K., Meyuhas O., Perry R. P., Johnson L. F. Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol Cell Biol. 1982 Jun;2(6):685–693. doi: 10.1128/mcb.2.6.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Helling R. B., Goodman H. M., Boyer H. W. Analysis of endonuclease R-EcoRI fragments of DNA from lambdoid bacteriophages and other viruses by agarose-gel electrophoresis. J Virol. 1974 Nov;14(5):1235–1244. doi: 10.1128/jvi.14.5.1235-1244.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holmgren R., Corces V., Morimoto R., Blackman R., Meselson M. Sequence homologies in the 5' regions of four Drosophila heat-shock genes. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3775–3778. doi: 10.1073/pnas.78.6.3775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hung M. C., Wensink P. C. Sequence and structure conservation in yolk proteins and their genes. J Mol Biol. 1983 Mar 15;164(4):481–492. doi: 10.1016/0022-2836(83)90046-3. [DOI] [PubMed] [Google Scholar]
  19. Hung M. C., Wensink P. C. The sequence of the Drosophila melanogaster gene for yolk protein 1. Nucleic Acids Res. 1981 Dec 11;9(23):6407–6419. doi: 10.1093/nar/9.23.6407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ingolia T. D., Craig E. A. Primary sequence of the 5' flanking regions of the Drosophila heat shock genes in chromosome subdivision 67B. Nucleic Acids Res. 1981 Apr 10;9(7):1627–1642. doi: 10.1093/nar/9.7.1627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kim C. H., Warner J. R. Messenger RNA for ribosomal proteins in yeast. J Mol Biol. 1983 Mar 25;165(1):79–89. doi: 10.1016/s0022-2836(83)80243-5. [DOI] [PubMed] [Google Scholar]
  22. Klemenz R., Geiduschek E. P. The 5' terminus of the precursor ribosomal RNA of Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Jun 25;8(12):2679–2689. doi: 10.1093/nar/8.12.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  25. McDonell M. W., Simon M. N., Studier F. W. Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J Mol Biol. 1977 Feb 15;110(1):119–146. doi: 10.1016/s0022-2836(77)80102-2. [DOI] [PubMed] [Google Scholar]
  26. Monk R. J., Meyuhas O., Perry R. P. Mammals have multiple genes for individual ribosomal proteins. Cell. 1981 May;24(2):301–306. doi: 10.1016/0092-8674(81)90319-6. [DOI] [PubMed] [Google Scholar]
  27. Mount S. M. A catalogue of splice junction sequences. Nucleic Acids Res. 1982 Jan 22;10(2):459–472. doi: 10.1093/nar/10.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pearson N. J., Fried H. M., Warner J. R. Yeast use translational control to compensate for extra copies of a ribosomal protein gene. Cell. 1982 Jun;29(2):347–355. doi: 10.1016/0092-8674(82)90151-9. [DOI] [PubMed] [Google Scholar]
  29. Pearson N. J., Haber J. E. Changes in regulation of ribosomal protein synthesis during vegetative growth and sporulation of Saccharomyces cerevisiae. J Bacteriol. 1980 Sep;143(3):1411–1419. doi: 10.1128/jb.143.3.1411-1419.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pearson N. J., Haber J. E. Changes in regulation of ribosomal protein synthesis during vegetative growth and sporulation of Saccharomyces cerevisiae. J Bacteriol. 1980 Sep;143(3):1411–1419. doi: 10.1128/jb.143.3.1411-1419.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Pierandrei-Amaldi P., Campioni N., Beccari E., Bozzoni I., Amaldi F. Expression of ribosomal-protein genes in Xenopus laevis development. Cell. 1982 Aug;30(1):163–171. doi: 10.1016/0092-8674(82)90022-8. [DOI] [PubMed] [Google Scholar]
  32. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  33. Rave N., Crkvenjakov R., Boedtker H. Identification of procollagen mRNAs transferred to diazobenzyloxymethyl paper from formaldehyde agarose gels. Nucleic Acids Res. 1979 Aug 10;6(11):3559–3567. doi: 10.1093/nar/6.11.3559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Ricciardi R. P., Miller J. S., Roberts B. E. Purification and mapping of specific mRNAs by hybridization-selection and cell-free translation. Proc Natl Acad Sci U S A. 1979 Oct;76(10):4927–4931. doi: 10.1073/pnas.76.10.4927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  36. Rubin G. M., Spradling A. C. Genetic transformation of Drosophila with transposable element vectors. Science. 1982 Oct 22;218(4570):348–353. doi: 10.1126/science.6289436. [DOI] [PubMed] [Google Scholar]
  37. Santon J. B., Pellegrini M. Expression of ribosomal proteins during Drosophila early development. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5649–5653. doi: 10.1073/pnas.77.10.5649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Seif I., Khoury G., Dhar R. A rapid enzymatic DNA sequencing technique: determination of sequence alterations in early simian virus 40 temperature sensitive and deletion mutants. Nucleic Acids Res. 1980 May 24;8(10):2225–2240. doi: 10.1093/nar/8.10.2225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Snyder M., Hunkapiller M., Yuen D., Silvert D., Fristrom J., Davidson N. Cuticle protein genes of Drosophila: structure, organization and evolution of four clustered genes. Cell. 1982 Jul;29(3):1027–1040. doi: 10.1016/0092-8674(82)90466-4. [DOI] [PubMed] [Google Scholar]
  40. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  41. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  42. Spradling A. C., Rubin G. M. Transposition of cloned P elements into Drosophila germ line chromosomes. Science. 1982 Oct 22;218(4570):341–347. doi: 10.1126/science.6289435. [DOI] [PubMed] [Google Scholar]
  43. Vaslet C. A., O'Connell P., Izquierdo M., Rosbash M. Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster. Nature. 1980 Jun 26;285(5767):674–676. doi: 10.1038/285674a0. [DOI] [PubMed] [Google Scholar]
  44. Weiss Y. C., Vaslet C. A., Rosbash M. Ribosomal protein mRNAs increase dramatically during Xenopus development. Dev Biol. 1981 Oct 30;87(2):330–339. doi: 10.1016/0012-1606(81)90156-1. [DOI] [PubMed] [Google Scholar]
  45. Wong Y. C., O'Connell P., Rosbash M., Elgin S. C. DNase I hypersensitive sites of the chromatin for Drosophila melanogaster ribosomal protein 49 gene. Nucleic Acids Res. 1981 Dec 21;9(24):6749–6762. doi: 10.1093/nar/9.24.6749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Woolford J. L., Jr, Hereford L. M., Rosbash M. Isolation of cloned DNA sequences containing ribosomal protein genes from Saccharomyces cerevisiae. Cell. 1979 Dec;18(4):1247–1259. doi: 10.1016/0092-8674(79)90236-8. [DOI] [PubMed] [Google Scholar]

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