Summary
During Drosophila early development the translation of ribosomal protein mRNAs is regulated specifically and coordinately. In this study we assayed for changes of ribosomal protein rp49 gene expression in flies transformed with extra copies of the gene. RNA blot analysis revealed that the rp49 transcript was overrepresented in most of the transformed fly lines: flies carrying three times more genes than the wild type contained up to seven times more mRNA. The abundance of other ribosomal protein mRNAs was not affected. Despite the large differences in rp49 mRNA content, the proportion of the rp49 mRNA which was associated with polysomes during oogenesis and early embryogenesis did not differ significantly from the wild type, implying that rp49 protein is overproduced in the transgenic flies. The results indicate that the basis for coordinate r-protein gene expression lies in the intrinsic properties of r-protein genes, rather than in a dynamic system that separately modulates the expression of individual genes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abovich N, Gritz L, Tung I, Rosbash M (1985) Effect of RP51 gene dosage alterations on ribosome synthesis in Saccharomyces cerevisiae. Mol Cell Biol 5:3429–3435
Al-Atia GR, Fruscoloni P, Jacobs-Lorena M (1985) Translational regulation of mRNAs for ribosomal proteins during early Drosophila development. Biochemistry 24:5798–5803
Baum EZ, Hyman LE, Wormington WM (1988) Post-translational control of ribosomal protein L1 accumulation in Xenopus oocytes. Dev Biol 126:141–149
Bozzoni I, Fragapane P, Annesi F, Pierandrei-Amaldi P, Amaldi F, Beccari E (1984) Expression of two Xenopus laevis ribosomal protein genes in injected frog oocytes. J Mol Biol 180:987–1005
Donovan DM, Pearson NJ (1986) Transcriptional regulation of ribosomal proteins during a nutritional upshift in Saccharomyces cerevisiae. Mol Cell Biol 6:2429–2435
Draper DE (1987) Translational regulation of ribosomal proteins in Escherichia coli. In: Ilan J (ed) Translational regulation of gene expression. Plenum, New York, pp 1–26
Faliks D, Meyuhas O (1982) Coordinate regulation of ribosomal protein mRNA level in regenerating rat liver. Study with the corresponding mouse cloned cDNAs. Nucleic Acids Res 10:789–801
Fruscoloni P, Al-Atia G, Jacobs-Lorena M (1983) Translational regulation of a specific gene during oogenesis and embryogenesis of Drosophila. Proc Natl Acad Sci USA 80:3359–3363
Fyrberg EA, Kindle KL, Davidson N, Sodja A (1980) The actin genes of Drosophila: a dispersed multigene family. Cell 19:365–378
Gantt JS, Key JL (1985) Coordinate expression of ribosomal protein mRNAs following auxin treatment of soybean hypocotyls. J Biol Chem 260:6175–6181
Hough-Evans BR, Jacobs-Lorena M, Cummings MR, Britten RJ, Davidson EH (1980) Complexity of RNA in eggs of Drosophila melanogaster and Musca domestica. Genetics 95:81–94
Jacobs-Lorena M, Fried H (1987) Translational regulation of ribosomal protein gene expression in eukaryotes. In: Ilan J (ed) Translational regulation of gene expression. Plenum, New York, pp 63–85
Kay MA, Jacobs-Lorena M (1985) Selective translational regulation of ribosomal protein gene expression during early development of Drosophila melanogaster. Mol Cell Biol 35:3583–3592
Kay MA, Zhang J-Y, Jacobs-Lorena M (1988) Identification and germline transformation of the ribosomal protein rp21 gene of Drosophila: Complementation analysis with the Minute QIII locus reveals nonidentity. Mol Gen Genet 213:354–358
Kongswan K, Qiang Y, Vincent A, Frisardi MC, Rosbash M, Lengyel JA, Merriam J (1985) A Drosophila Minute gene encodes a ribosomal protein. Nature 217:555–557
Levis R, Hazelrigg T, Rubin GM (1985) Effects of genomic position on the expression of transduced copies of the white gene of Drosophila. Science 229:558–560
Mager WH (1988) Control of ribosomal protein gene expression. Biochem Biophys Acta 949:1–15
Maicas E, Pluthero FG, Friesen JD (1988) The accumulation of three yeast ribosomal proteins under conditions of excess mRNA is determined primarily by fast protein decay. Mol Cell Biol 8:169–175
O'Connell P, Rosbash M (1984) Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucleic Acids Res 12:5495–5513
Pierandrei-Amaldi P, Campioni N, Beccari E, Bozzoni I, Amaldi F (1982) Expression of ribosomal-protein genes in Xenopus laevis development. Cell 30:163–171
Pierandrei-Amaldi P, Bozzoni I, Cardinali B (1988) Expression of the gene for ribosomal protein L1 in Xenopus embryos: alteration of gene dosage by microinjection. Genes Dev 2:23–31
Qian S, Zhang JY, Kay M, Jacobs-Lorena M (1987) Structural analysis of the Drosophila rpAl gene, a member of the eukaryotic ‘A’ type ribosomal protein family. Nucleic Acids Res 15:987–1003
Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251
Spradling AC, Rubin G (1983) The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 34:47–57
Tsay Y-F, Thompson JR, Rotenberg MO, Larkin JC, Woolford JL Jr (1988) Ribosomal protein synthesis is not regulated at the translational level in Saccharomyces cerevisiae: balanced accumulation of ribosomal proteins L16 and rp59 is mediated by turnover of excess protein. Genes Dev 2:664–676
Wakimoto BT, Kalfayan LJ, Spradling AC (1986) Developmentally regulated expression of Drosophila chorion genes introduced at diverse chromosomal positions. J Mol Biol 187:33–45
Warner JR, Mitra G, Schwindinger WF, Studeny M, Fried HM (1985) Saccharomyces cerevisiae coordinates accumulation of yeast ribosomal proteins by modulating mRNA splicing, translational initiation, and protein turnover. Mol Cell Biol 5:1512–1521
Author information
Authors and Affiliations
Additional information
Communicated by B.H. Judd
Rights and permissions
About this article
Cite this article
Tamate, H.B., Patel, R.C., Riedl, A.E. et al. Overproduction and translational regulation of rp49 ribosomal protein mRNA in transgenic Drosophila carrying extra copies of the gene. Molec. Gen. Genet. 221, 171–175 (1990). https://doi.org/10.1007/BF00261717
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00261717