Summary
Minute loci represent a class of about 50 different Drosophila genes that appear to be functionally related. These genes may code for components of the protein synthetic apparatus. While one Minute locus has been recently shown to code for a ribosomal protein, it is not yet known whether any of the other Minute loci also code for ribosomal proteins. We have addressed this question by a combined molecular and genetic approach. In this report, a cloned DNA encoding the ribosomal protein rp21 is partially characterized. The rp21 gene maps to the same region (region 80 of chromosome 3L) as the temperature-sensitive Minute QIII gene. Using P-element mediated transformation, the rp21 gene was transformed into the germline of Drosophila. RNA blot experiments revealed that the transformed gene is expressed in transgenic flies. However, genetic complementation analysis indicated that the QIII locus and the rp21 gene are not identical. Implications of these findings for the relationship between Minutes and ribosomal protein genes are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Al-Atia GR, Fruscoloni P, Jacobs-Lorena M (1985) Translational regulation of mRNAs for ribosomal proteins during early Drosophila development. Biochemistry 24:5798–5803
Anderson KV, Lengyel JA (1979) Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol 70:217–231
Ballinger DG, Pardue ML (1983) The control of protein synthesis during heat shock in Drosophila cells involves altered polypeptide elongation rates. Cell 33:103–114
Biessmann H, Kuger P, Schropfer C, Spindler E (1981) Molecular cloning and preliminary characterization of a Drosophila melanogaster gene from a region adjacent to the centrometric bheterochromatin. Chromosoma 82:493–503
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
Brehme KS (1939) A study of the effect on the development of Minute mutations in Drosophila melanogaster. Genetics 24:131–159
Brehme KS (1941) Development of the Minute phenotype in Drosophila melanogaster. A comparative study of the growth of three Minute mutants. J Exp Zool 88:135–160
Burns DK, Stark BC, Macklin MD, Chooi WY (1984) Isolation and characterization of cloned DNA sequences containing ribosomal protein genes of Drosophila melanogaster. Mol Cell Biol 4:2643–2652
Chooi WY (1980) Purification of Drosophila ribosomal proteins. Isolation of proteins S8, S13, S14, S16, S19, S20/L24, S22/L26, S24/, S25/S27, S26, S29, L4, L10/L11, L12, L13, L16, L18, L19, L27, L1, L7/8, L9, and L11. Biochemistry 19:3469–3476
Chooi WY, Sabatini LM, Macklin M, Fraser D (1980) Group fractionation and determination of the number of ribosomal subunit proteins from Drosophila melanogaster embryos. Biochemistry 19:1425–1433
Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44:871–877
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 10:789–800
Farnsworth MW (1957a) Effects of the homozygous Minute-IV deficiency on the development of Drosophila melanogaster. Genetics 42:7–18
Farnsworth MW (1957b) Effects of homozygous first, second, and third chromosome Minutes on the development of Drosophila melanogaster. Genetics 42:19–27
Fried HM, Nam HG, Loecher S, Teem J (1985) Characterization of yeast strains with conditionally expressed variants of ribosomal protein genes tcml and cyh2. Mol Cell Biol 5:99–108
Geyer PK, Meyuhas O, Perry RP, Johnson LF (1982) Regulation of ribosomal protein mRNA content and translation in growth-stimulated mouse fibroblasts. Mol Cell Biol 2:685–693
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
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 Press, 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 5:3582–3592
Kay MA, Jacobs-Lorena M (1987) Developmental genetics of ribosome synthesis in Drosophila. Trends Genet 3:347–351
Kongsuwan K, Qiang Y, Vincent A, Frisardi MC, Rosbash M, Lengyel JA, Merriam J (1985) A Drosophila Minute gene encodes a ribosomal protein. Nature 317:555–558
Lindsley DL, Grell EH (1968) Genetic variations of Drosophila melanogaster. Carnegie Inst Washington
Lindsley DL, Sandler L, Baker BS, Carpenter ATC, Denell RE, Hall JC, Jacobs PA, Miklos GLG, Davis BK, Gethmann RC, Hardy RW, Hessler A, Miller SM, Nozawa H, Parry DM, Gould-Somero M (1972) Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71:157–184
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Morata G, Ripoll P (1975) Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev Biol 42:211–221
Pearson NJ, Fried HM, Warner JR (1982) Yeast use translational control to compensate for extra copies of a ribosomal protein gene. Cell 29:347–355
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
Qian S, Zhang J-Y, Kay MA, Jacobs-Lorena M (1987) Structural analysis of the Drosophila rpA1 gene, a member of the eucaryotic “A” type ribosomal protein family. Nucleic Acids Res 15:987–1003
Rubin GM, Spradling AC (1982) Genetic transformation with transposable element vectors. Science 218:348–353
Rubin GM, Spradling AC (1983) Vectors for P-element mediated transfer in Drosophila. Nucleic Acids Res 11:6341–6351
Ruddell A, Jacobs-Lorena M (1984) Preferential expression of actin genes during oogenesis of Drosophila. Dev Biol 105:115–120
Schultz J (1929) The Minute reaction in the development of Drosophila melanogaster. Genetics 14:366–419
Sinclair DAR, Suzuki DT, Grigliatti TA (1981) Genetic and developmental analysis of a temperature-sensitive Minute mutation of Drosophila melanogaster. Genetics 97:581–606
Vaslet CA, O'Connell P, Izquierdo M, Rosbash M (1980) Isolation and mapping of a cloned ribosomal protein gene of Drosophila melanogaster. Nature 285:674–676
Vogelstein B, Gillespie D (1979) Preparative and analytical purification of DNA from agarose. Proc Natl Acad Sci USA 76:615–619
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
Kay, M.A., Zhang, J.Y. & Jacobs-Lorena, M. 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 (1988). https://doi.org/10.1007/BF00339602
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00339602