Skip to main content
Log in

Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae: multiple trans-acting nuclear genes exert specific effects on expression of each of the cytochrome c oxidase subunits encoded on mitochondrial DNA

  • Original Articles
  • Published:
Current Genetics Aims and scope Submit manuscript

Summary

Fourteen nuclear complementation groups of mutants that specifically affect the three mitochondrially-encoded subunits of yeast cytochrome c oxidase have been characterized. Genes represented by these complementation groups are not required for mitochondrial transcription, transcript processing, or translation per se but are required for the expression of one of the three genes — COX1, COX2, or COX3 — which encode the cytochrome c oxicase subunits I, II, or III, respectively. Five of these genes affect the biogenesis of cytochrome c oxidase subunit I, 3 affect the biogenesis of subunit II, 3 affect the biogenesis of subunit III and 3 affect the biogenesis of both cytochrome c oxidase subunit I and cytochrome b, the product of COB. Among the 5 complementation groups of mutants that affect the expression of COX1, 2 lack COX1 transcripts, 1 produces incompletely processed COX1 transcripts, and 2 contain normal levels of normal-sized COX1 transcripts. In contrast, all 3 complementation groups which affect the expression of COX2 and all 3 complementation groups which affect the expression of COX3 exhibit no, or little, detectable difference with respect to the wild type pattern of transcripts. The 3 complementation groups which affect the expression of both COX1 and COB all have aberrant COX1 and COB transcript patterns. These findings indicate that multiple trans-acting nuclear genes are required for specific expression of each COX gene encoded on mitochondrial DNA and suggest that their products act at different steps in the expression of these mitochondrial genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arrese MR, Vojensky D, Mattoon JR (1982) Biochem Biophys Res Commun 107:848–855

    Google Scholar 

  • Atkinson KD (1985) Genetics 111:1–6

    Google Scholar 

  • Bertrand H, Bridge P, Collins RA, Garriga G, Lambowitz A (1982) Cell 25:517–526

    Google Scholar 

  • Bonitz SG, Coruzzi G, Thalenfeld BE, Tzagoloff A, Macino G (1980) J Biol Chem 255:11927–11941

    Google Scholar 

  • Cobon GS, Beilhary MW, Linnane AW, Nagley P (1982) Curr Genet 5:97–104

    Google Scholar 

  • Costanzo MC, Seaver EC, Fox TD (1986) EMBO J 5:3637–3641

    Google Scholar 

  • Coruzzi G, Bonitz S, Thalenfeld BE, Tzagoloff A (1981) J Biol Chem 256:12780–12887

    Google Scholar 

  • Denhardt DT (1966) Biochem Biophys Res Commun 23:641–646

    Google Scholar 

  • Dieckman CL, Pape LK, Tzagoloff A (1982) Proc Natl Acad Sci USA 79:1805–1809

    Google Scholar 

  • Dieckmann CL, Tzagoloff A (1985) J Biol Chem 260:1513–1520

    Google Scholar 

  • Ebner E, Menucci L, Schatz G (1973) J Biol Chem 248:5360–5368

    Google Scholar 

  • Falcone C, Agostinelli M, Frontali L (1983) J Bacteriol 153:1125–1132

    Google Scholar 

  • Faye G, Simon M (1983) Cell 32:77–87

    Google Scholar 

  • Guerry P, LeBlanc DJ, Falkow S (1973) J Bacteriol 116:1064–1066

    Google Scholar 

  • Hensgens LAM, Arnberg AC, Roosendaal E, VanderHorst G, Van der Deen R, Van Ommen GJB, Grivell LA (1983) J Mol Biol 164:35–58

    Google Scholar 

  • Kloeckener-Gruissem B (1985) PhD dissertation. University of Colorado, Boulder, Colorado

  • Lobouesse M, Dujardin G, Slonimski PP (1985) Cell 41:133–143

    Google Scholar 

  • Lazowska J, Jacq C, Slonimski PP (1980) Cell 22:333–348

    Google Scholar 

  • Macino G, Tzagoloff A (1980) Cell 20:507–517

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning, Cold Spring Harbor Laboratory, Cold Spring Harbor New York

    Google Scholar 

  • McEwen JE, Cameron VL, Poyton RO (1985) J Bacteriol 161:831–835

    Google Scholar 

  • McEwen JE, Cumsky MG, Ko C, Power SD, Poyton RO (1984) J Cell Biochem 24:229–242

    Google Scholar 

  • McEwen JE, Ko C, Kloeckener-Gruissem B, Poyton RO (1986) J Biol Chem 261:11872–11879

    Google Scholar 

  • McGraw P, Tzagoloff A (1983) J Biol Chem 258:9459–9468

    Google Scholar 

  • McKee EE, Poyton RO (1984) J Biol Chem 259:9320–9331

    Google Scholar 

  • McKee EE, McEwen JE, Poyton RO (1984) J Biol Chem 259:9332–9338

    Google Scholar 

  • Michaelis G, Mannhaupt G, Pratje E, Fisher E, Naggert J, Schweizer E (1982) Mitochondrial translation products in nuclear respiratory-deficient pet mutants of Saccharomyces cerevisaae. In: Slonimski PP, Borst P, Attardi G (eds) Mitochondrial genes. Cold Spring Harbor Laboratory, Cold Spring Harbor New York, pp 311–321

    Google Scholar 

  • Mueller PP, Reif MK, Zonghou S, Sengsteg C, Mason TL, Fox TD (1984) J Mol Biol 175:431–452

    Google Scholar 

  • Myers AM, Pape LK, Tzagoloff A (1985) EMBO J 4:2087–2092

    Google Scholar 

  • Needleman RB, Tzagoloff A (1975) Anal Biochem 64:545–549

    Google Scholar 

  • Nobrega FG, Tzagoloff A (1980) J Biol Chem 255:9828–9837

    Google Scholar 

  • Pape LK, Koerner TJ, Tzagoloff A (1985) J Biol Chem 260:15362–15370

    Google Scholar 

  • Pillar T, Lang BF, Steinberger I, Vogt B, Kaudewitz F (1983) J Biol Chem 258:7954–7959

    Google Scholar 

  • Power SD, Lochrie MA, Sevarino KA, Patterson TE, Poyton RO (1984) J Biol Chem 259:6564–6570

    Google Scholar 

  • Poyton RO, Bellus G, Kerner AL (1982) In: Martonosi A (ed) Membranes and transport, vol 1. Plenum, New York, pp 237–247

    Google Scholar 

  • Pratje E, Mannhaupt G, Michaelis G, Beyreuther K (1983) EMBO J 2:1049–1054

    Google Scholar 

  • Pratje E, Schulz R, Schnierer S, Michaelis G (1979) Mol Gen Genet 176:411–415

    Google Scholar 

  • Rodel G, Korte A, Kaudewitz F (1985) Curr Genet 9:641–648

    Google Scholar 

  • Sherman F, Fink GR, Hicks JB (1983) Methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor New York

    Google Scholar 

  • Thalenfeld BE, Hill J, Tzagoloff A (1983) J Biol Chem 258:610–615

    Google Scholar 

  • Thalenfeld BE, Tzagoloff A (1980) J Biol Chem 255:6173–6180

    Google Scholar 

  • Tzagoloff A, Akai A, Needleman RB (1975) J Biol Chem 250:8228–8235

    Google Scholar 

  • Weiss-Brummer B, Guba R, Haid A, Schweyen RJ (1979) Curr Genet 1:75–83

    Google Scholar 

  • Williamson DH, Fennel DJ (1979) Methods Cell Biol 12:335–351

    Google Scholar 

  • Zennaro E, Grimaldi L, Balducci G, Frontali L (1985) Eur J Biochem 147:191–196

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kloeckener-Gruissem, B., McEwen, J.E. & Poyton, R.O. Nuclear functions required for cytochrome c oxidase biogenesis in Saccharomyces cerevisiae: multiple trans-acting nuclear genes exert specific effects on expression of each of the cytochrome c oxidase subunits encoded on mitochondrial DNA. Curr Genet 12, 311–322 (1987). https://doi.org/10.1007/BF00405753

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00405753

Key words

Navigation