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Clonal analysis of two mutations in the large subunit of RNA polymerase II of Drosophila

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Summary

Two mutations in the gene, RpII215, were analyzed to determine their effects on cell differentiation and proliferation. The mutations differ in that one, RpII215 ts(ts), only displays a conditional recessive lethality, while the other, RpII215 Ubl (Ubl), is a recessive lethal mutation that also displays a dominant mutant phenotype similar to that caused by the mutation Ultrabithorax (Ubx). Ubl causes a partial transformation of the haltere into a wing; however, this transformation is more complete in flies carrying both Ubl and Ubx. The present study shows that patches of Ubl/- tissue in gynandromorphs are morphologically normal. Cuticle that has lost the wild-type copy of the RpII215 locus fails to show a haltere to wing transformation, nor does it show the synergistic enhancement of Ubx by Ubl. We conclude that an interaction between the two RpII215 alleles, Ubl and RpII215 +, is responsible for the mutant phenotype. Gynandromorphs carrying the ts allele, when raised at permissive temperature, display larger patches of ts/- cuticle than expected, possibly indicating that the proliferation of ts/+ cells is reduced. This might result from an antagonistic interaction between different RpII215 alleles. Classical negative complementation does not appear to be the cause of the antagonistic interaction described above, as only one RpII215 subunit is thought to be present in an active multimeric polymerase enzyme. We have therefore coined the term ‘negative heterosis’ to describe the aforementioned interactions.

We also observed that the effects of mutationally altered RNA polymerase II on somatic cells are different from its effects on germ cells. Mutant somatic cells (either Ubl/- or ts/-, the latter shifted to restrictive temperature) reduce cell proliferation, but otherwise do not appear to disrupt cell differentiation. However, mutant germ cells often differentiate into morphologically abnormal oocytes.

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References

  • akam M, Moore H, Cox A (1984) Ultrabithorax mutations map to distinct sites within the bithorax complex of Drosophila. Nature 309:635–637

    Google Scholar 

  • Amati P, Blasi F, Diporzio U, Riccio A, Traboni C (1975) Hamster α-amanitine-resistant RNA polymerase II able to transcribe polyoma virus genome in somatic cell hybrids. Proc Natl Acad Sci USA 72:753–757

    Google Scholar 

  • Arking R (1975) Temperature-sensitive cell-lethal mutants of Drosophila: Isolation and characterization. Genetics 80:519–537

    Google Scholar 

  • Artavanis-Tsakonas S, Muskavitch MAT Yedvobnick B (1983) Molecular cloning of Notch a locus affecting neurogenesis in Drosophila melanogaster. Proc Natl Acad Sci USA 80:1977–1981

    Google Scholar 

  • Bender W, Akam M, Karch F, Beachy PA, Peifer M, Spierer P, Lewis EB, Hogness DS (1983) Molecular genetics of the bithorax complex in Drosophila melanogaster. Science 221:23–29

    Google Scholar 

  • Bryant RE, Adelberg EA, Magee PT (1977) Properties of an altered RNA polymerase II activity from an α-amanitin-resistant mouse cell line. Biochemistry 16:4237–4244

    Google Scholar 

  • Catcheside DG, Lea DE (1945) Dominant lethals and chromosome breaks in ring-X chromosomes of Drosophila melanogaster. J Genet 47:25–40

    Google Scholar 

  • Chambon P (1975) Eukaryotic nuclear RNA polymerase. Annu Rev Biochem 44:613–638

    Google Scholar 

  • Chan VL, Whitmore GF, Siminovitch L (1972) Mammalian cells with altered forms of RNA polymerase II. Proc Natl Acad SCi USA 69:3119–3123

    Google Scholar 

  • Cochet-Meilhac M, Chambon P (1974) Animal DNA-dependent RNA polymerases. II. Mechanism of the inhibition of RNA polymerases B by amatoxins. Biochim Biophys Acta 353:160–184

    Google Scholar 

  • Garcia-Bellido A (1972) Some parameters of mitotic recombination in Drosophila melanogaster. Mol Gen Genet 115:54–72

    Google Scholar 

  • Greenleaf AL, Borsett LM, Jiamachello PF, Coulter DE (1979) α-amanitin-resistant D. melanogaster with an altered RNA polymerase II. Cell 18:613–622

    Google Scholar 

  • Greenleaf AL, Weeks JR, Voelker RA, Ohnishi S, Dickson B (1980) Genetic and biochemical characterization of mutants at an RNA polymerase II locus in D. melanogaster. Cell 21:785–792

    Google Scholar 

  • Greenleaf AL (1983) Amanitin-resistant RNA polymerase II mutations are in the enzyme's largest subunit. J Biol Chem 258:13403–13406

    Google Scholar 

  • Guialis A, Beatty BG, Ingles CJ, Crerar MM (1977) Regulation of RNA polymerase II activity in α-amanitin-resistant CHO hybrid cells. Cell 10:53–60

    Google Scholar 

  • Guialis A, Morrison KE, Ingles CJ (1979) Regulated synthesis of RNA polymerase II polypeptides in Chinese hamster ovary cell line. J Biol Chem 254:4171–4176

    Google Scholar 

  • Kramer A, Bautz EKF (1981) Immunological relatedness of subunits of RNA polymerase II from insects and mammals. Eur J Biochem 117:449–455

    Google Scholar 

  • Lobban PE, Siminovitch L, Ingles CJ (1976) The RNA polymerase II of an α-amanitin-resistant chinese hamster ovary cell line. Cell 8:65–70

    Google Scholar 

  • Morata G, Ripoll P (1975) Minutes: Mutants of Drosophila autonomously affecting cell division rate. Dev Biol 42:211–221

    Google Scholar 

  • Mortin MA, Lefevre Jr G (1981) An RNA polymerase II mutation in Drosophila melanogaster that mimics Ultrabithorax. Chromosoma 82:237–247

    Google Scholar 

  • Mortin MA, Kaufman TC (1982) Developmental genetics of a temperature-sensitive RNA polymerase II mutation in Drosophila melanogaster. Mol Gen Genet 187:120–125

    Google Scholar 

  • Mortin MA, Kaufman TC (1984) Developmental effects of a temperature-sensitive RNA polymerase II mutation in Drosophila melanogaster. Dev Biol 103:343–354

    Google Scholar 

  • Mortin MA (1983) Analysis of a temperature-sensitive mutation in a gene encoding a subunit of RNA polymerase II in Drosophila. Ph.D dissertation Indiana University

  • Perrimon N, Gans M (1983) Clonal analysis of the tissue specificity of recessive female sterile mutations of Drosophila melanogaster using a dominant female sterile mutation Fs(1)K1237. Dev Biol 100:365–373

    Google Scholar 

  • Polya GM (1973) Transcription. In: Stewart PR, Letham DS (eds) The Ribonucleic Acids. Springer-Verlag, New York, pp 7–58

    Google Scholar 

  • Roeder RG (1976) Eukaryotic nuclear RNA polymerases. In: Losick R, Chamberlin M (eds) RNA Polymerase. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, pp 285–329

    Google Scholar 

  • Scott MP, Weiner AJ, Hazelrigg TI, Polisky BA, Pirrotta V, Scalenghe F, Kaufman TC (1983) The molecular organization of the Antennapedia locus of Drosophila. Cell 35:763–776

    Google Scholar 

  • Simpson P, Schneiderman HA (1975) Isolation of temperature sensitive mutations blocking clone development in Drosophila melanogaster, and the effects of a temperature sensitive cell lethal mutation on pattern formation of imaginal discs. Wilhelm Roux Arch 178:247–275

    Google Scholar 

  • Simpson P (1976) Analysis of the compartments of the wing of Drosophila melanogaster mosaic for a temperature-sensitive mutation that reduces mitotic rate. Dev Biol 54:100–115

    Google Scholar 

  • Somers DG, Pearson ML, Ingles CJ (1975) Regulation of RNA polymerase II activity in a mutant rat myoblast cell line resistant to α-amanitin. Nature 253:372–374

    Google Scholar 

  • Turner FR, Mahowald AP (1976) Scanning electron microscopy of Drosophila melanogaster embryogenesis. I. The structure of the egg envelope and the formation of the cellular blastoderm. Dev Biol 50:95–108

    Google Scholar 

  • Vaisius AC, Wieland T (1982) Formation of a single phosphodiester bond by RNA polymerase B from calf thymus is not inhibited by α-amanitin. Biochemistry 21:3097–3101

    Google Scholar 

  • Windsor B, Lacroute F, Ruet A, Sentenac A (1979) Isolation and characterisation of a strain of Saccharomyces cerevisiae deficient in in vitro polymerase B(II) activity. Mol Gen Genet 173:145–151

    Google Scholar 

  • Young RA, Davis RW (1983) Yeast RNA polymerase II genes: Isolation with antibody probes. Science 222:778–782

    Google Scholar 

  • Yura T, Ishihama A (1979) Genetics of Bacterial RNA polymerases. Annu Rev Genet 13:59–97

    Google Scholar 

  • Zalokar M, Erk I, Santamaria P (1980) Distribution of ring-X chromosomes in the blastoderm of gynandromorphic D. melanogaster. Cell 19:133–141

    Google Scholar 

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Communicated by M.M. Green

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Mortin, M.A., Perrimon, N. & Bonner, J.J. Clonal analysis of two mutations in the large subunit of RNA polymerase II of Drosophila . Mol Gen Genet 199, 421–426 (1985). https://doi.org/10.1007/BF00330753

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  • DOI: https://doi.org/10.1007/BF00330753

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