Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Dec 1;88(23):10716–10720. doi: 10.1073/pnas.88.23.10716

Functional analysis in yeast of cDNA coding for the mitochondrial Rieske iron-sulfur protein of higher plants.

J T Huang 1, F Struck 1, D F Matzinger 1, C S Levings 3rd 1
PMCID: PMC53001  PMID: 1961737

Abstract

cDNA clones coding for the nuclear-encoded mitochondrial Rieske iron-sulfur protein (RISP) have been isolated from maize and tobacco. Complementation analysis of hybrid proteins consisting of different domains of plant and yeast RISPs showed that the carboxyl two-thirds of the plant protein is functionally equivalent to that of the yeast protein. The amino terminus of the RISP, however, seems to be species specific because this region is not interchangeable between plant and yeast proteins. Complementation analysis of hybrid proteins also identified a structurally conserved domain probably essential for the function of bc1 complex RISPs. A specific domain from the plant RISP was found to cause temperature-sensitive respiratory growth in yeast. We have demonstrated that yeast can serve as a model system to study the structural and functional relationships of plant gene products that are enzymatic components of the mitochondrial respiratory chain.

Full text

PDF
10716

Images in this article

10717Image
on p.10717
10718Image
on p.10718
10718Image
on p.10718
10718Image
on p.10718
10719Image
on p.10719
10719Image
on p.10719

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beckmann J. D., Ljungdahl P. O., Lopez J. L., Trumpower B. L. Isolation and characterization of the nuclear gene encoding the Rieske iron-sulfur protein (RIP1) from Saccharomyces cerevisiae. J Biol Chem. 1987 Jun 25;262(18):8901–8909. [PubMed] [Google Scholar]
  2. Beckmann J. D., Ljungdahl P. O., Trumpower B. L. Mutational analysis of the mitochondrial Rieske iron-sulfur protein of Saccharomyces cerevisiae. I. Construction of a RIP1 deletion strain and isolation of temperature-sensitive mutants. J Biol Chem. 1989 Mar 5;264(7):3713–3722. [PubMed] [Google Scholar]
  3. Bowler C., Alliotte T., Van den Bulcke M., Bauw G., Vandekerckhove J., Van Montagu M., Inzé D. A plant manganese superoxide dismutase is efficiently imported and correctly processed by yeast mitochondria. Proc Natl Acad Sci U S A. 1989 May;86(9):3237–3241. doi: 10.1073/pnas.86.9.3237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chaumont F., O'Riordan V., Boutry M. Protein transport into mitochondria is conserved between plant and yeast species. J Biol Chem. 1990 Oct 5;265(28):16856–16862. [PubMed] [Google Scholar]
  5. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  6. Daum G., Böhni P. C., Schatz G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem. 1982 Nov 10;257(21):13028–13033. [PubMed] [Google Scholar]
  7. Fu W., Japa S., Beattie D. S. Import of the iron-sulfur protein of the cytochrome b.c1 complex into yeast mitochondria. J Biol Chem. 1990 Sep 25;265(27):16541–16547. [PubMed] [Google Scholar]
  8. Gabellini N., Sebald W. Nucleotide sequence and transcription of the fbc operon from Rhodopseudomonas sphaeroides. Evaluation of the deduced amino acid sequences of the FeS protein, cytochrome b and cytochrome c1. Eur J Biochem. 1986 Feb 3;154(3):569–579. doi: 10.1111/j.1432-1033.1986.tb09437.x. [DOI] [PubMed] [Google Scholar]
  9. González-Halphen D., Vázquez-Acevedo M., García-Ponce B. On the interaction of mitochondrial complex III with the Rieske iron-sulfur protein (subunit V). J Biol Chem. 1991 Feb 25;266(6):3870–3876. [PubMed] [Google Scholar]
  10. Güssow D., Clackson T. Direct clone characterization from plaques and colonies by the polymerase chain reaction. Nucleic Acids Res. 1989 May 25;17(10):4000–4000. doi: 10.1093/nar/17.10.4000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harnisch U., Weiss H., Sebald W. The primary structure of the iron-sulfur subunit of ubiquinol-cytochrome c reductase from Neurospora, determined by cDNA and gene sequencing. Eur J Biochem. 1985 May 15;149(1):95–99. doi: 10.1111/j.1432-1033.1985.tb08898.x. [DOI] [PubMed] [Google Scholar]
  12. Hartl F. U., Schmidt B., Wachter E., Weiss H., Neupert W. Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of ubiquinol-cytochrome c reductase. Cell. 1986 Dec 26;47(6):939–951. doi: 10.1016/0092-8674(86)90809-3. [DOI] [PubMed] [Google Scholar]
  13. Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem. 1985;54:1015–1069. doi: 10.1146/annurev.bi.54.070185.005055. [DOI] [PubMed] [Google Scholar]
  14. Hauska G., Hurt E., Gabellini N., Lockau W. Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta. 1983 Jul 15;726(2):97–133. doi: 10.1016/0304-4173(83)90002-2. [DOI] [PubMed] [Google Scholar]
  15. Hendrick J. P., Hodges P. E., Rosenberg L. E. Survey of amino-terminal proteolytic cleavage sites in mitochondrial precursor proteins: leader peptides cleaved by two matrix proteases share a three-amino acid motif. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4056–4060. doi: 10.1073/pnas.86.11.4056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hill J. E., Myers A. M., Koerner T. J., Tzagoloff A. Yeast/E. coli shuttle vectors with multiple unique restriction sites. Yeast. 1986 Sep;2(3):163–167. doi: 10.1002/yea.320020304. [DOI] [PubMed] [Google Scholar]
  17. Huang J., Hack E., Thornburg R. W., Myers A. M. A yeast mitochondrial leader peptide functions in vivo as a dual targeting signal for both chloroplasts and mitochondria. Plant Cell. 1990 Dec;2(12):1249–1260. doi: 10.1105/tpc.2.12.1249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hurd H. K., Roberts C. W., Roberts J. W. Identification of the gene for the yeast ribonucleotide reductase small subunit and its inducibility by methyl methanesulfonate. Mol Cell Biol. 1987 Oct;7(10):3673–3677. doi: 10.1128/mcb.7.10.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kallas T., Spiller S., Malkin R. Primary structure of cotranscribed genes encoding the Rieske Fe-S and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5794–5798. doi: 10.1073/pnas.85.16.5794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  22. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  23. Lin T. Y., Markhart A. H. Temperature Effects on Mitochondrial Respiration in Phaseolus acutifolius A. Gray and Phaseolus vulgaris L. Plant Physiol. 1990 Sep;94(1):54–58. doi: 10.1104/pp.94.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mack D. H., Sninsky J. J. A sensitive method for the identification of uncharacterized viruses related to known virus groups: hepadnavirus model system. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6977–6981. doi: 10.1073/pnas.85.18.6977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Malkin R., Bearden A. J. Membrane-bound iron-sulfur centers in photosynthetic systems. Biochim Biophys Acta. 1978 Oct 23;505(2):147–181. doi: 10.1016/0304-4173(78)90011-3. [DOI] [PubMed] [Google Scholar]
  26. Mullis K., Faloona F., Scharf S., Saiki R., Horn G., Erlich H. Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol. 1986;51(Pt 1):263–273. doi: 10.1101/sqb.1986.051.01.032. [DOI] [PubMed] [Google Scholar]
  27. Nishikimi M., Hosokawa Y., Toda H., Suzuki H., Ozawa T. Cloning and sequence analysis of a cDNA encoding the Rieske iron-sulfur protein of rat mitochondrial cytochrome bc1 complex. Biochem Biophys Res Commun. 1989 Feb 28;159(1):19–25. doi: 10.1016/0006-291x(89)92398-x. [DOI] [PubMed] [Google Scholar]
  28. Rieske J. S. Composition, structure, and function of complex III of the respiratory chain. Biochim Biophys Acta. 1976 Sep 27;456(2):195–247. doi: 10.1016/0304-4173(76)90012-4. [DOI] [PubMed] [Google Scholar]
  29. Saiki R. K., Scharf S., Faloona F., Mullis K. B., Horn G. T., Erlich H. A., Arnheim N. Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science. 1985 Dec 20;230(4732):1350–1354. doi: 10.1126/science.2999980. [DOI] [PubMed] [Google Scholar]
  30. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  32. Schmitz U. K., Lonsdale D. M. A yeast mitochondrial presequence functions as a signal for targeting to plant mitochondria in vivo. Plant Cell. 1989 Aug;1(8):783–791. doi: 10.1105/tpc.1.8.783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schägger H., Borchart U., Machleidt W., Link T. A., Von Jagow G. Isolation and amino acid sequence of the 'Rieske' iron sulfur protein of beef heart ubiquinol:cytochrome c reductase. FEBS Lett. 1987 Jul 13;219(1):161–168. doi: 10.1016/0014-5793(87)81210-3. [DOI] [PubMed] [Google Scholar]
  34. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Trumpower B. L. Cytochrome bc1 complexes of microorganisms. Microbiol Rev. 1990 Jun;54(2):101–129. doi: 10.1128/mr.54.2.101-129.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Trumpower B. L., Edwards C. A. Purification of a reconstitutively active iron-sulfur protein (oxidation factor) from succinate . cytochrome c reductase complex of bovine heart mitochondria. J Biol Chem. 1979 Sep 10;254(17):8697–8706. [PubMed] [Google Scholar]
  37. Trumpower B. L. Function of the iron-sulfur protein of the cytochrome b-c1 segment in electron-transfer and energy-conserving reactions of the mitochondrial respiratory chain. Biochim Biophys Acta. 1981 Dec 4;639(2):129–155. doi: 10.1016/0304-4173(81)90008-2. [DOI] [PubMed] [Google Scholar]
  38. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES