Abstract
Mitochondria posses their own ribosomes responsible for the synthesis of a small number of proteins encoded by the mitochondrial genome. In yeast,Saccharomyces cerevisiae, the two ribosomal RNAs and a single ribosomal protein, Varl, are products of mitochondrial genes, and the remaining approximately 80 ribosomal proteins are encoded in the nucleus. The mitochondrial translation system is dispensable in yeast, providing an excellent experimental model for the molecular genetic analysis of the fundamental properties of ribosomes in general as well as adaptations required for the specialized role of ribosomes in mitochondria. Recent studies of the peptidyl transferase center, one of the most highly conserved functional centers of the ribosome, and the Varl protein, an unusual yet essential protein in the small ribosomal subunit, have provided new insight into conserved and divergent features of the mitochondrial ribosome.
Similar content being viewed by others
References
Myers, A. M., Pape, L. K. and Tzagoloff A. (1985) Mitochondrial protein synthesis is required for maintenance of intact mitochondrial genomes inSaccharomyces cerevisiae. EMBO J.4: 2087–2092
Kitakawa, M., and Isono, K. (1991) The mitochondrial ribosomes. Biochimie73: 813–825
Mason, T. L., and Sirum-Connolly K. (1996) Expression of rRNA genes in mitochondria and chloroplasts. In: Ribosomal RNA: Structure, Evolution, Processing, and Function in Protein Biosynthesis, pp. 421–449. Zimmermann, R. A. and Dahlberg, A. E. (ed.), RCR Press, Boca Raton, Florida
Fox, T. D. (1996) Genetics of mitochondrial translation. In: Translational Control, pp. 733–758, Hershey, J. W. B., Matthews, M. B., and Sonenberg, N. (eds), Cold Spring Harbor Press, Cold Spring Harbor, New York.
Grivell, L. A. (1995) Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit. Rev. Biochem. Molec. Biol.30: 121–164
Dieckmann, C. L. and Staples, R. R. (1984) Regulation of mitochondrial gene expression inSaccharomyces cerevisiae. Int. Rev. Cytol.152: 145–181
Noller, H. F. (1993) Peptidyl transferase: protein, ribonucleoprotein, or RNA? J Bacteriol.175: 5297–5300
Noller, H. F. (1993) tRNA-rRNA interactions and peptidyl transferase. Faseb J.7: 87–89
Lieberman, K. R., and Dahlberg, A. E. (1995) Ribosome-catalyzed peptide-bond formation. In: Progress in Nucleic Acid Research and Molecular Biology, vol. 50, pp. 1–23, Cohn W. E. and Moldave, K. (eds). Academic Press Inc, 525 B Street, Suite 1900, San Diego, California 92101-4495
Garrett, R. A. and Rodriguez-Fonseca, C. (1996) The peptidyl transferase center. In: Ribosomal RNA: Structure, Evolution, Processing, and Function in Protein Biosynthesis pp. 327–355, Zimmermann, R. A. and Dahlberg A. E. (eds.), CRC Press, Boca Raton, Florida
Noller, H. F., Hoffarth, V. and Zimniak, L. (1992) Unusual resistance of peptidyl transferase to protein extraction procedures [see comments]. Science256: 1416–1419
Garrels, J. (1995) YPD—A database for the proteins ofSaccharomyces cerevisiae. Nucl. Acids Res.24: 46–49.
Pan, C., Sirum-Connolly, K., and Mason, T. L. (1993) Essential features of the peptidyl transferase center in the yeast mitochondrial ribosome. In: The Translational Apparatus. Structure, Function, Regulation, Evolution, pp. 587–598, Nierhaus, K. H., Franceschi, F., Subramanian, A. R., Erdmann, V. A. and Wittmann-Liebold B. (eds), Plenum Press, New York
Fearon, K., and Mason, T. L. (1988) Structure and regulation of a nuclear gene inSaccharomyces cerevisiae that specifies MRP7, a protein of the large subunit of the mitochondrial ribosome. Molec. Cell. Biol.8: 3636–3646
Pan, C. and Mason, T. L. (1995) Identification of the yeast nuclear gene for the mitochondrial homologue of bacterial ribosomal protein L16. Nucl. Acids Res.23: 3673–3677
Egebjerg, J., Christiansen, J. and Garrett, R. A. (1991) Attachment sites of primary binding protein-L1, protein-L2 and protein-L23 on 23-S ribosomal RNA ofEscherichia-coli. J. Molec. Biol.222: 251–264
Cooperman, B.S., Wooten, T., Romero, D. P. and Traut R. R. (1966) Histidine 229 in protein L2 is apparently essential for 50S peptidyl transferase activity. Biochem. Cell. Biol.73: 1087–1094
Pan C. (1994) Molecular genetic dissection of nuclear genes for proteins in the peptidyl transferase center of the yeast mitochondrial ribosome, PhD Thesis, University of Massachusetts
Wower, J., Wower, I. K., Kirillov, S. V., Rosen, K. V., Hixon, S. S. and Zimmermann, R. A. (1996) Peptidyl transferase and beyond. Biochem. Cell. Biol.73: 1041–1047
Wower, J., Sylvers, L. A., Rosen, K. V., Hixson, S. S. and Zimmermann, R. A. (1993) A model of the tRNA binding sites on theEscherichia coli ribosome. In: The Translational Apparatus. Structure, Function, Regulation, Evolution, pp. 455–464, Nierhaus, K. H., Franceschi, F., Subramanian, A. R., Erdmann, V. A. and Wittmann-Liebold B. (eds), Plenum Press, New York
Walleczek, J., Martin, T., Redl, B. Stoffler-Meilicke, M. and Stoffler, G. (1989) Comparative cross-linking study on the 50S ribosomal subunit fromEscherichia coli. Biochemistry28: 4099–4105
Walleczek J., Redl B, Stoffler-Meilicke M. and Stoffler G. (1989) Protein-protein cross-linking of the 50S ribosomal subunit ofEscherichia coli using 2-iminothiolane. Identification of cross-links by immunoblotting techniques. J. Biol. Chem.264: 4231–4237
Redl, B., Walleczek, J., Stoffler-Meilicke, M., and Stoffler, G. (1989) Immunoblotting analysis of protein-protein crosslinks within the 50S ribosomal subunit ofEscherichia coli. A study using dimethylsuberimidate as crosslinking reagent. Eur. J. Biochem.181: 351–356
Garrett R. A., Muller, S., Spiercer P. and Zimmermann R. A. (1974) Binding of 50S ribosomal subunit proteins to 23S RNA ofEscherichia coli. J. Molec. Biol.88 553–557
Wower I., Wower J., Meinke M. and Brimacombe R. (1981) The use of 2-iminothiolane as an RNA-protein cross-linking agent inEscherichia coli ribosomes, and the localization on 23S RNA of sites cross-linked to proteins L4, L6, L21, L23, L27 and L29. Nucl. Acids Res.9: 4285–4302
Gulle H., Hoppe E., Osswald M., Greuer B., Brimacombe R. and Stoffler G. (1988) RNA-protein cross-linking inEscherichia coli 50S ribosomal subunits; determination of sites on 23S RNA that are cross-linked to proteins L2, L4, L24 and L27 by traetment with 2-iminothiolane. Nucl. Acids Res.16: 815–832
Osswald M., Greuer B. and Brimacombe R. (1990) Localization of a series of RNA-protein cross-link sites in the 23S and 5S ribosomal RNA fromEscherichia coli, induced by treatment of 50S subunits with three different bifunctional reagents. Nucl. Acids Res.18: 6755–6760
Schulze H. and Nierhaus K. H. (1982) Minimal set of ribosomal components for reconstitution of the peptidyltransferase activity. EMBO J.1: 609–613
Dabbs E. R., Hasenbank R., Kastner B., Pak K.-H., Wartusch B. and Stoffler G. (1983) Immunological studies ofEscherichia coli mutants lacking one or two ribosomal proteins. Molec. Gen. Genet.192: 301–308
Fearon K. (1989) Nuclear genes inSaccharomyces cerevisiae that encode proteins of the large subunit of the mitochondrial ribosome., Ph.D. Thesis, University of Massachusetts
Huff M. O., Hanic-Joyce P. J., Dang H., Rodrigues L. A. and Ellis S. R. (1993) Two inactive fragments derived from the yeast mitochondrial ribosomal protein MrpS28 function in trans to support ribosome assembly and respiratory growth. J. Molec. Biol.233: 597–605
Thurlow D. L., Mason T. L. and Zimmermann R. A. (1984) 5S RNA-like structures in large ribosomal subunit RNAs of fungal mitochondria. FEBS Letters173: 277–282
Lang B. F., Cedergren R. and Gray M. W. (1987) The mitochondrial genome of the fission yeast,Schizosaccharomyces pombe. Sequence of the large-subunit ribosomal RNA gene, comparison of potential secondary structure in fungal mitochondrial large-subunit rRNAs and evolutionary considerations. Eur. J. Biochem.169: 527–537
Dontsova O., Tishkov V., Dokudovskaya, S. Bogdanov A., Doring T., Rinkeappel J., Thamm S., Greuer B., and Brimacombe R. (1994) Stem-loop IV of 5S rRNA lies close to the peptidyltransferase center. Proc. Natl. Acad. Sci. USA91: 4125–4129
Dokudovskaya S., Dontsova O., Shpanchenko O., Bogdanov A. and Brimacombe R. (1996) Loop IV of 5S ribosomal RNA has contacts both to domain II and to domain V of the 23S RNA. RNA2: 146–152
Moore P. B. (1966) The structure and function of 5S ribosomal RNA. In: Ribosomal RNA: Structure, Evolution, Processing, and Function in Protein Biosynthesis, pp. 199–236 Zimmermann R. A. and Dahlberg A. E. (eds) CRC Press, Boca Raton, Florida
Sirum-Connolly K., Peltier J. M., Crain P. F., McCloskey J. A. and Mason T. L. (1995) Implications of a functional large ribosomal RNA with only three modified nucleotides. Biochimie77: 30–39
Klootwijik J., Klein I. and Grivell L. A. (1975) Minimal post-transcriptional modification of yeast mitochondrial ribosomal RNA. J. Molec. Biol.97: 337–350
Bakin A., Lane B. G. and Ofengand J. (1994) Clustering of pseudouridine residues around the peptidyltransferase center of yeast cytoplasmic and mitochondrial ribosomes. Biochemistry.33: 13475–13483
Sirum-Connolly K. and Mason T. L. (1993) Functional requirement of a site-specific ribose methylation in ribosomal RNA. Science262; 1886–1889
Moazed D. and Noller H. F. (1989) Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell57: 585–597
Samaha R. R., Green R. R. and Noller H. F. (1995) A base pair between tRNA and 23S rRNA in the peptidyle transferase centrer of the ribosome. Nature377: 309–314
Krzyzosiak W., Denman R., Nurse K., Hellman W., Boublik M. Gehrke C. W., Agris P. F. and Ofengand J. (1987) In vitro synthesis of 16S ribosomal RNA containing single base changes and assembly into a functional 30S ribosome. Biochemistry26: 2353–2364
Pinkham J. L., Dudley A. M. and Mason T. L. (1994) T7 RNA polymerase-dependent expression ofCOXII in yeast mitochondria. Molec. Cell. Biol.14: 4643–4652
Lane B. G., Ofengand J. and Gray M. W. (1995) Pseudouridine and 2′-O-methlated nucleosides. Significance of their selective occurrence in rRNA domains that function in ribosome-catalyzed synthesis of the peptide bounds in proteins. Biochimie77: 7–15
Maden B. E. H., Corbett M. E., Heeney P. A., Pugh K. and Ajuh P. M. (1985) Classical and novel approaches to the detection and localization of the numerous modified nucleotides in eukaryotic ribosomal RNA. Biochimie77: 22–29
Kiss-Laszlo Z., Henry Y., Bachellerie J.-P., Caizergues-Ferrer M. and Kiss T. (1996) Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell85: 1077–1088
Sanchirico M., Tzellas A., Fox T. D., Conrad-Webb H., Perlman P. S. and Mason T. L. (1995) Relocation of the unusualVAR1 gene from the mitochondrion to the nucleus. Biochem. Cell. Biol.73: 987–995
Groot G. S. P., Mason T. L. and VanHarten-Loosbroek N. (1979) Varl is associated with the small ribosomal subunit of mitochondrial ribosomes in yeast. Molec. Gen. Genet.174: 339–342
Terpstra P. and Butow R. A. (1979) The role of varl in the assembly of yeast mitochondrial ribosomes. J. Biol. Chem.254: 12662–12669
Douglas M. G. and Butow R. A. (1976) Variant forms of mitochondrial translation products in yeast: evidence for location of determinants on mitochondrial DNA. Proc. Natl. Acad. Sci. U.S.A.73: 1083–1086
Butow R. A., Perlman P. S. and Grossman L. I. (1985) The unusualvarl gene of yeast mitochondrial DNA. Science228: 1496–1501
Hudspeth M. E., Ainley W. M., Shumard D. S., Butow R. A. and Grossman L. I. (1982) Location and structure of theVAR1 gene on yeast mitochondrial DNA: nucleotide sequence of the 40.0 allele. Cell30: 617–626
Murphy K., Choo K. B., Macreadie I. Marzuki S., Lukins H. B., Nagley P. and Linnane A. W. (1980) Biogenesis of mitochondria: a temperature sensitivity mutation affecting the mitochondrially synthesized Varl protein ofSaccharomyces cerevisiae. Arch. Biochem. Biophys.203: 260–270
Zassenhaus H. P. and Perlman P. S. (1982) Respiration deficient mutants in the A/T-rich region on the yeast mitochondrial DNA containing thevar1 gene. Curr. Genetics,6: 179–188
Butow R. A., Perlman P. S. and Grossman L. I. (1985) The unusualVAR1 gene of yeast mitochondrial DNA. Science228: 1496–1501
Davis S. C. and Ellis S. R. (1995) Incorporation of the yeast mitochondrial ribosomal protein Mrp2 into ribosomal subunits requires the mitochondrially encoded Var1 protein. Molec. Gen. Genet.247: 379–386
Haffter P., McMullin T. W. and Fox T. D. (1990) A genetic link between an mRNA-specific translational activator and the translation system in yeast mitochondria. Genetics,125: 495–503
Haffter P. and Fox T. D. (1992) Suppression of carboxy-terminal truncations of the yeast mitochondrial mRNA-specific translational activator PET122 by mutations in two new genes, MRP17 and PET127. Molec. Gen. Genet.235: 64–73
McMullin T. W., Haffter P. and Fox T. D. (1990) A novel small-subunit ribosomal protein of yeast mitochondria that interacts functionally with an mRNA-specific translational activator. Molec. Cell. Biol.10: 4590–4595
Conrad-Webb H., Perlman P. S., Zhu H., and Butow R. A. (1990) The nuclearSUV3-1 mutation affects a variety of post-transcriptional processes in yeast mitochondria. Nucl. Acids Res.18: 1369–1376
Steele D. F., Butler C. A. and Fox T. D. (1996) Expression of a recoded nuclear gene inserted into yeast mitochondrial DNA is limited by mRNA-specific translational activation. Proc. Natl. Acad. Sci. USA93: 5253–5257
Attardi G. and Schatz G. (1988) Biogenesis of mitochondria. A. Rev. Cell. Biol.4: 289–333
Claros M. G., Perea J., Shu Y., Samatey F. A., Popot J.-L. and Jacq C. (1995) Limitations to in vitro import of hydrophobic proteins into yeast mitochondria: the case of a cytoplasmically synthesized apocytochromeb. Eur. J. Biochem.228: 762–771
Grohmann L., Graack H. R., Kruft V., Choli T, Goldschmidtreisin S. and Kitakawa M. (1991) Extended N-terminal sequencing of proteins of the large ribosomal subunit from yeast mitochondria. FEBS Letters284: 51–56
Olsen G. J., Overbeek R., Larsen N., Marsh T. L., Mccaughey M. J., Maciukenas M. A., Kuan W. M., Macke T. J., Xing Y. Q. and Woese C. R. (1992) The Ribosomal Database Project. Nucl. Acids Res.20: 2199–2200
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mason, T.L., Pan, C., Sanchirico, M.E. et al. Molecular genetics of the peptidyl transferase center and the unusual Var1 protein in yeast mitochondrial ribosomes. Experientia 52, 1148–1157 (1996). https://doi.org/10.1007/BF01952114
Issue Date:
DOI: https://doi.org/10.1007/BF01952114