Summary
We have isolated about five hundred temperature-sensitive mutants specific for the mitochondrial functions. Their growth on glycerol is defective at 36°C and/or 20°C. While most of the mutations were nuclearly inherited, about thirty were found to be of mitochondrial origin.
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1)
Four mitochondrial mutations (three cryosensitive, one thermosensitive) were localized close to chloramphenicol and erythromycin resistance loci of the mitochondrial DNA, that is in the region coding for the 23 S ribosomal RNA. One of the mutation interfered with the expression of the chloramphenicol resistance gene.
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2)
A dozen nuclear mutations were isolated from a strain which is labelled with mitochondrial drug resistance markers (chloramphenicol, erythromycin, and paromomycin). Among the temperature sensitive respiratory deficient mutants, we have selected the mutations that supress the resistant phenotypes. We describe two non allelic such mutations, one being cryosensitive, the other thermosensitive. Both supress the expression of the mitochondrial chloramphenicol resistance gene. The temperature sensitive growth on glycerol and the modified antibiotic phenotype segregated together as a single recessive mutation.
A biochemical study of these mutants is presented in a joint paper, confirming their presumed ribosomal nature.
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References
Bogorad, L., Davidson, J.N., Hanson, M.R.: Genes affecting erythromycin resistance and sensitivity of chlamydomonas reinhardii chloroplast ribosomes. In: Genetics and giogenesis of chloroplasts and mitochondria, Th. Bücher et al. (eds.), pp. 61–67. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press 1976
Bolotin-Fukuhara, M., Faye, G., Fukuhara, H.: Localization of some mitochondrial mutations in relation to transfer and ribosomal RNA genes in Saccharomyces cerevisiae. In: The Genetic function of mitochondrial DNA, G. Saccone and A.M. Kroon (eds.), pp. 242–250. Amsterdam, The Netherlands: North-Holland Biomedical Press 1976
Bolotin-Fukuhara, M., Faye G., Fukuhara, H.: Temperature-sensitive respiratory-deficient mitochondrial mutations. Isolation and genetic mapping. Mol. Gen. Genet. 152, 295–305 (1977)
Borst, P., Grivell, L.A.: Mitochondrial ribosomes. FEBS Lett. 13, 73–88 (1971)
Bos, J.L., Heyting, C., Borst, P., Arnberg, A.C., Van Bruggen, E.F.J.: An insert in the single gene for the large ribosomal RNA in yeast mitochondrial DNA. Nature 275, 336–338 (1978)
Coen, D., Deutsch, J., Netter, P., Petrochilo, E., Slonimski, P.P.: Mitochondrial genetics. I: Methodology and Phenomenology. Symposia of the Society for Experimental Biology, No. 24, pp. 449–496, Cambridge: Cambridge University Press 1970
Collins, R.A., Bertrand, H.: Nuclear suppressors of the [poky] cytoplasmic mutants in Neurospora crassa. III. Effects on other cytoplasmic mutants and on mitochondrial assembly in [poky]. Mol. Gen. Genet. 161 267–273 (1978)
Davidson, J.N., Hanson M.R. Bogorad, L.: Erythromycin resistance and the chloroplast ribosome in C. reinhardii. Genetics 89, 281–296 (1978)
Devenish, R.J., English, K.J., Hall, R.M., Linnane, A.W., Lukins, H.B.: Biogenesis of mitochondria 49-Identification and mapping of a new mitochondrial locus (tsr 1) which maps within the polar region of the yeast mitochondrial genome. Mol. Gen. Genet. 161, 251–259 (1978)
Dujon, B., Bolotin-Fukuhara, M., Coen, D., Deutsch, J., Netter, P., Slonimski, P.P., Weill, L.: Mitochondrial genetics XI. Mutations at the mitochondrial locus ω affecting the recombination of mitochondrial genes in Saccharomyces cerevisiae. Mol. Gen. Genet. 143, 131–165 (1976)
Dujon, B., Slonimski, P.P. Weill, L.: Mitochondrial genetics IX. A model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78, 415–437 (1974)
Faye, G., Dennebouy, N., Kujawa, E., Jacq, C.: Inserted sequence in the mitochondrial 23 S ribosomal RNA gene of the yeast Saccharomyces cerevisiae Mol. Gen. Genet. 168, 101–110 (1979)
Faye, G., Kujawa, H., Dujon, B. Bolotin-Fukuhara, M., Wolf, C., Fukuhara, H., Slonimski, P.P.: Localization of the gene coding for the mitochondrial 16 S ribosomal RNA using rho- mutants of Saccharomyces cerevisiae. J. Mol. Biol. 99, 203–217 (1975)
Faye, G., Kujawa, C., Fukuhara, H.: Physical and genetic organization of petite and grande yeast mitochondrial DNA. IV. In vivo transcription products of mitochondrial DNA and localization of 23 S ribosomal RNA in petite mutants of Saccharomyces cerevisiae. J. Mol. Biol. 88, 185–203 (1974)
Fukuhara, H., Faye, G., Michel, F., Lazowska, G., Deutsch, J., Bolotin-Fukuhara, M., Slonimski, P.P.: Physical and genetic organization of petite and grande yeast mitochondrial DNA. I. Studies by RNA-DNA hybridization Mol. Gen. Genet. 130 215–238 (1974)
Gilham N.W., Boynton, J.E., Harris, E.H., Fox, S.B., Bolen, P.L.: Genetic control of chloroplast biogenesis in chlamydomonas. In: Genetics and biogenesis of chloroplasts and mitochondria, Th. Bücher et al. (eds.), pp 69–76. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press 1976
Grivell, L.A., Netter, P., Borst, P., Slonimski, P.P.: Mitochondrial antibiotic resistance in yeast: ribosomal mutants resistant to chloramphenicol, erythromycin and spiramycin. Biochim. Biophys. Acta. 312, 358–367 (1973)
Groot, G.S.P.: The biosynthesis of mitochondrial ribosomes in Saccharomyces cerevisiae. In: The biogenesis of mitochondria, A.M. Kroon and S. Saccone (eds.), pp. 443–452. New York: Academic Press 1974
Jaskunas S.R., Nomura, M., Davies, J.: Genetics of bacterial ribosomes. In: Ribosomes M. Nomura et al. (eds.), pp. 333–368. Cold Spring Harbor: Cold Spring Harbor Laboratory 1974
Lambowitz, A.M.: The poky mutant of Neurospora crassa. In: Genetics and biogenesis of chloroplast and mitochondria, Th Bücher et al. (eds.), pp 713–720. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press 1976
Lancashire, W.E.: Mitochondrial mutations conferring heat or cold sensitivity in Saccharomyces cerevisiae. In: Genetics and biogenesis of chloroplast and mitochondria, Th Bücher et al. (eds.), pp. 481–491. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press 1976
La Polla R.J., Lambowitz, A.M.: Mitochondrial ribosome assembly in N. crassa. Chloramphenicol inhibits the maturation of small ribosomal subunits. J. Mol. Biol. 116, 189–206 (1977)
Lukins, H.B., English, J.T., Spithill, T.W., Devenish, R.J., Hall, R.M., Nagley, P., Linnane, A.W.: Biochemical characterization of a temperature conditional mutant having a mutation in the ω controlled region of the yeast mitochondrial genome and effects of deletion of the mutation on mitochondrial recombination. In: Mitochondria 1977-Genetics and biogenesis of mitochondria, W. Bandlow et al. (eds.), pp. 107–122. Berlin: De Gruyter 1977
Mason, T., Boerner, P., Biron, C.: The use of double mutant strains containing heat- and cold-sensitive mutations in studies of mitochondrial biogenesis. In: Genetics and biogenesis of chloplasts and mitochondria, Th. Bücher et al. (eds.), pp. 239–246. Amsterdam, The Netherlands: Elsevier/North-Holland Biomedical Press 1976
Nomura, M., Held, W.A.: Reconstitution of ribosomes: studies of ribosome structure, function and assembly. In: Ribosomes, M. Nomura et al. (eds.), pp 193–224, Cold Spring Harbor: Cold Spring Harbor Laboratory 1974
Pellegrini, M., Manning, J., Davidson, N.: Sequence arrangement of the rDNA of Drosophila melanogaster. Cell 10, 213–224 (1977)
Reinjders, L., Keisen, C.M., Grivell, L.A. Borst, P.: Hybridization studies with yeast mitochondrial RNA's. Biochim Biophys. Acta 272, 396–407 (1972)
Rochaix, J.D., Malnoe, P.: Anatomy of the chloroplast ribosomal DNA of chlamydomonas reinhardii. Cell 15, 661–670 (1978)
Sanders, J.P.M., Heyting, C., Borst, P.: The organization of genes in yeast mitochondrial DNA. I. The genes for large and small ribosomal RNA are far apart. Biochem. Biophys. Res. Commun. 65, 699–707 (1975)
Schweyen, R.J., Kaudewitz, F: Formation of rho- petites in yeast. I. Multifactorial crosses (rho+xrho+) involving a mutation conferring temperature-sensitivity of rho factor stability. Mol. Gen. Genet. 149, 311–322 (1976)
Singh, A., Mason, T.L., Zimmerman, R.A: A cold-sensitive cytoplasmic mutation of Saccharomyces cerevisiae affecting assembly of the mitochondrial 50 S ribosomal subunit. Mol. Gen. Genet. 161, 143–151 (1978)
Slonimski, P.P., Tzagoloff, A.: Localization in yeast mitochondrial DNA of mutations expressed in a deficiency of cytochrome oxidase and of coenzyme QH2-cytochrome c reductase. Eur. J. Biochem. 61, 27–41 (1976)
Sor, E., Faye, G.: Mitochondrial and nuclear mutations that affect the biogenesis of the mitochondrial ribosomes of yeast. II. Biochemical data. Mol. Gen. Genet. 177, 47–56 (1979)
Tzagoloff, A., Akai, A., Needleman, R.: Assembly of the mitochondrial membrane system: isolation of nuclear and cytoplasmic mutants of Saccharomyces cerevisiae with specific defects in mitochondrial functions. J. Bacteriol. 122, 826–831 (1975)
Wellauer, P.K., Dawid, I.: The structural organization of ribosomal DNA in Drosophila melanogaster. Cell 10, 193–212 (1977)
White, R., Hogness, D.: R- Loop mapping of the 18 S and 28 S sequences in the long and short repeating units of Drosophila melanogaster rDNA. Cell 10, 177–192 (1977)
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Communicated by F. Kaudewitz
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Bolotin-Fukuhara, M. Mitochondrial and nuclear mutations that affect the biogenesis of the mitochondrial ribosomes of yeast. Molec. Gen. Genet. 177, 39–46 (1979). https://doi.org/10.1007/BF00267251
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DOI: https://doi.org/10.1007/BF00267251