Summary
Fifty-nine mutations that restrict suppressor efficiency were selected in the fungus Podospra anserina using four different screening methods. Previous genetic analysis has shown that these antisuppressors lie in six loci and that they could be similar to ribosomal restrictive mutations known in Escherichia coli. The present study deals with the response of two of them, AS1-1 and AS6-1, to paromomycin and low temperature both in vivo and in vitro. The data demonstrate that ribosomes of the mutant and double-mutant strains are equally resistant to the ambiguity effect of paromomycin. These data are the first demonstration of mutations that increase translational fidelity in a eucaryotic organism.
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References
Begueret J, Perrot M, Crouzet M (1977) Ribosomal proteins in the fungus Podospora anserina: evidence for an electrophoretically altered 60S protein in a cycloheximide resistant mutant. Mol Gen Genet 156:141–144
Bollen A, Cabezon T, Topisirovic L, De Wilde M, Villaroel R, Herzog A (1976) Ribosomal mutations interfering with translational fidelity. In: Zelinka and Balan (eds.) Ribosomes and RNA metabolism, vol 2. Publ. House Slovak Acad Sciences, Bratislava, pp 55–66
Bryan LE, van den Elzen HM (1977) Effects of membrane energy mutations and cations on streptomycin and gentamicin accumulation by bacteria: a model for entry of streptomycin and gentamicin in susceptible and resistant bacteria. Antimicrob Agents Chemother 12:163–177
Coddington A, Fluri R (1977) Characterization of the ribosomal proteins from Schizosaccharomyces pombe by two-dimensional poly-acrylamide gel electrophoresis: demonstration that cycloheximide resistant strain, cyhl, has an altered 60S ribosomal protein. Mol Gen Genet 158:93–100
Coppin-Raynal E (1977) Ribosomal suppressors and antisuppressors in Podospora anserina: resistance to cycloheximide. J Bacteriol 131:876–883
Coppin-Raynal E (1980) Ribosomal suppressors and antisuppressors in Podospora anserina: altered susceptibility to paromomycin and relationships between genetic and phenotypic suppression. Biochem Genet (in press)
Crouzet M, Begueret J (1978) Cold sensitivity of a double-mutant strain combining two ribosomal mutations in the ascomycete Podospora anserina. Mol Gen Genet 165:293–288
Crouzet M, Perrot M, Nogueira M, Begueret J (1978) Genetic and biochemical analysis of cycloheximide resistance in the fungus Podospora anserina. Biochem Genet 16:271–286
Dequard M, Couderc J-L, Legrain P, Belcour L, Picard-Bennoun M (1980) Search for ribosomal mutants in Podospora anserina: genetic analysis of mutants resistant to paromomycin. Biochem Genet 18:263–280
Edelmann P, Gallant J (1977) Mistranslation in E. coli. Cell 10:131–137
Elseviers D, Gorini L (1975) Direct selection of mutants restricting efficiency of suppression and misreading levels in E. coli B. Mol Gen Genet 137:277–287
Esser K (1974) Podospora anserina. In: King RC (ed) Handbook of genetics, vol 1. Plenum Press, New-York and London, pp 531–551
Friedman SM, Weinstein IB (1964) Lack of fidelity in the translation of synthetic polyribonucleotides. Proc Natl Acad Sci USA 52:988–996
Garvin RT, Gorini L (1975) A new gene for ribosomal restriction in Escherichia coli. Mol Gen Genet 137:73–78
Gorini L (1974) Streptomycin and misreading of the genetic code. In: Nomura M, Tissieres A, Lengyel P (eds) Ribosomes. Cold Spring Harbor, Laboratory, New-York, pp 791–803
Gupta RS, Schlessinger D (1976) Coupling of rates of transcription, translation and messenger ribonucleic acid degradation in streptomycin-dependant mutants of Escherichia coli. J Bacteriol 125:84–93
Hawthorne DC, Leupold U (1974) Suppressor mutations in yeast. Curr Top Microbiol Immunol 64:1–47
Kühberger R, Piepersberg W, Petzet A, Buckel P, Böck A (1979) Alteration of ribosomal protein L6 in gentamicin-resistant strains of E. coli. Effects on fidelity of protein synthesis. Biochemistry 18:187–193
Liebman SW, Cavenagh M (1980) An antisuppressor that acts on omnipotent suppressors in yeast. Genetics 95:49–61
Loftfield RB, Vanderjagt D (1972) The frequency of errors in protein synthesis. Biochem J 128:1353–1356
Mac Cready S, Cox BS (1973) Antisuppressors in yeast. Mol Gen Genet 124:305–320
Ninio J (1974) A semi-quantitative treatment of missense and non-sense suppression in the StrA and ram ribosomal mutants of E. coli. J Mol Biol 84:297–313
Palmer E, Wilhelm JM (1978) Mistranslation in an eucaryotic organism. Cell 13:329–334
Palmer E, Wilhelm JM, Sherman F (1979) Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature 277:148–150
Picard M (1973) Genetic evidence for a polycistronic unit of transcription in the complex locus “14” in Podospora anserina II-Genetic analysis of informational suppressors. Gen Res (Camb) 21:1–15
Picard-Bennoun M (1976) Genetic evidence for ribosomal antisupressors in Podospora anserina. Mol Gen Genet 147:299–306
Picard-Bennoun M, Coppin-Raynal E (1977) Une fonction ribosomique essentielle: le contrôle de la fidélité de la traduction. Physiol Veg 15:481–489
Picard-Bennoun M, Le Coze D (1980) Search for ribosomal mutants in Podospora anserina: genetic analysis of cold-sensitive mutants. Gen Res (Camb) 36:289–297
Piepersberg W, Geyl D, Hummel H, Böck A (1980) Physiology and biochemistry of bacterial ribosomal mutants. In: Genetics and evolution of transcriptional and translational apparatus. Kodansha Scientific, Tokyo, pp 359–377
Piepersberg W, Noseda V, Böck A (1979) Bacterial ribosomes with two ambiguity mutations: effects on translational fidelity on the response to aminoglycosides and on the rate of protein synthesis. Mol Gen Genet 171:23–34
Rizet G, Engelmann C (1949) Contribution à l'étude d'un ascomycète tétrasporé: Podospora anserina. Rey Cytol Biol Veget 2:202–304
Schlanger G, Friedman SM (1973) Ambiguity in a polypeptide-synthesizing extract from Saccharomyces cerevisiae. J Bacteriol 115:129–138
Singh A, Ursic D, Davies J (1979) Phenotypic suppression and misreading in Saccharomyces cerevisiae. Nature 277:146–148
Surguchov AP, Berestetskaya YuV, Fominykch ES, Pospelova EM, Smirnov VN, Ter-Avanesyan MD, Inge-Vechtomov SG (1980) Recessive suppression in yeast Saccharomyces cerevisiae is mediated by a ribosomal mutation. FEBS Lett 111:175–178
Szer W, Ochoa S (1964) Complexing ability and coding properties of synthetic polynucleotides J Mol Biol 8:823–834
Szybalski W, Mashima S (1959) Uptake of streptomycin by sensitive, resistant and dependent bacteria. Biochem Biophys Res Commun 1:149–154
Thorbjarnardottir SH, Magnusdottir RA, Eggertsson G, Kagan SA, Andresson OS (1978) Mutations determining generalized resistance to aminoglycoside antibiotics in Escherichia coli. Mol Gen Genet 161:89–98
Thuriaux P, Minet M, Hofer F, Leupold U, (1975) Genetic analysis of antisuppressor mutants in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 142:251–261
Wilhelm JM, Jessop JJ, Pettitt SE (1978b) Aminoglycoside antibiotics and eukaryotic protein synthesis: stimulation of errors in translation of natural messengers in extracts of cultured human cells. Biochemistry 17:1149–1153
Wilhelm JM, Pettitt SE, Jessop J (1978a) Aminoglycoside antibiotics and eukaryotic protein synthesis: structure-fonction relationships in the stimulation of miscreading with a wheat embryo system. Biochemistry 17:1143–1149
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Communicated by A. Böck
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Picard-Bennoun, M. Mutations affecting translational fidelity in the eucaryote Podospora anserina: Characterization of two ribosomal restrictive mutations. Molec. Gen. Genet. 183, 175–180 (1981). https://doi.org/10.1007/BF00270158
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DOI: https://doi.org/10.1007/BF00270158