Identification, cDNA sequence and deduced amino acid sequence of the mitochondrial Rieske iron-sulfur protein from the green alga Chlamydomonas reinhardtii Implications for protein targeting and subunit interaction

European Journal of Biochemistry

Volumn 237, Issue 3, 1996, Pages 792-799

  Atteia, Ariane ^a   Franzén, Lars Gunnar ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Chlamydomonas reinhardtii; Interaction with the bc1 complex; Mitochondria; Rieske iron sulfur protein; Targeting signal

Indexed keywords

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; FUNGI; MAMMALIA;

IRON SULFUR PROTEIN;

ALGA; AMINO ACID SEQUENCE; ARTICLE; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHLAMYDOMONAS REINHARDTII; DNA, COMPLEMENTARY; DNA, PROTOZOAN; ELECTRON TRANSPORT COMPLEX III; HUMANS; IRON-SULFUR PROTEINS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY;

EID: 0029890306     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0792p.x     Document Type: Article

References (57)

1. Amati, B., Goldschmidt-Clermont, M., Wallace, J. A. & Rochaix, J.-D. (1988) cDNA and deduced amino acid sequences of cytochrome c from Chlamydomonas reinhardtii: unexpected functional and phylogenetic implications, J. Mol. Biol. 28, 151-160.
2. Atteia, A. (1994a) Identification of mitochondrial respiratory proteins from the green alga Chlamydomonas reinhardtii, C. R. Acad. Sci. Ser. III Sci. Vie 317, 11-19.
3. Atteia, A. (1994b) Studies on the mitochondrial respiratory proteins from the unicellular green alga C. reinhardtii, PhD thesis, University of Paris VII.
4. Bennetzen, J. L. & Hall, B. D. (1982) Codon selection in yeast, J. Biol. Chem. 257, 3026-3031.
5. 1 complex in mammals and retained as a subunit in the complex, J. Biol. Chem. 268, 8387-8390.
6. 6f subunits. The Rieske iron-sulfur protein from Chlamydomonas reinhardtii is an extrinsic protein, J. Biol. Chem. 269, 7597-7602.
7. Buschlen, S., Choquet, Y., Kuras, R. & Wollman, F. A. (1991) Nucleotide sequences of the continuous and separated petA, petB and petD chloroplast genes in Chlamydomonas reinhardtii, FEBS Lett. 284, 257-262.
8. Chua, N.-H., Matlin, K. & Bennoun, P. (1975) A chlorophyll-protein complex lacking in photosystem I mutants of Chlamydomonas reinhardtii. J. Cell Biol. 67, 361-377.
9. Cocco, T., Lorusso, M., Sardanelli, A. M., Minuto, M., Ronchi, S., Tedeschi, G. & Papa, S. (1991) Structural and functional characteristics of polypeptide subunits of the bovine heart ubiquinol-cytochrome c reductase complex, Eur. J. Biochem. 195, 731-734.
10. 6f complex; structure of the lumen-side domain of cytochrome f, J. Bioenerg. Biomembr. 26, 31-47.
11. 1 complex of Rhodobacter capsulatus probed by site-directed mutagenesis, Biochemistry 31, 3342-3351.
12. de Boer, A. D. & Weisbeek, P. (1991) Chloroplast protein topogenesis: import, sorting and assembly, Biochim. Biophys. Acta 1071, 221-253.
13. de Vitry, C. (1994) Characterization of the gene of the chloroplast Rieske iron-sulfur protein in Chlamydomonas reinhardtii, J. Biol. Chem. 269, 7603-7609.
14. Emmermann, M., Clericus, M., Braun, H.-P., Mozo, T., Heins, L., Kruft, V. & Schmitz, U. K. (1994) Molecular features, processing and import of the Rieske iron-sulfur protein from potato mitochondria, Plant Mol. Biol. 25, 271-281.
15. Farah, J. A., Frank, G., Zuber, H. & Rochaix, J.-D. (1995) Cloning and sequencing of a cDNA encoding the photosystem I PsaD subunit from Chlamydomonas reinhardtii, Plant Physiol. (Bethesda) 107, 1485-1486.
16. Franzén, L.-G. & Falk, G. (1992) Nucleotide sequence of cDNA clones encoding the β subunit of mitochondrial ATP synthase from the green alga Chlamydomonas reinhardti: the precursor protein encoded by the cDNA contains both an N-terminal presequence and a C-terminal extension, Plant Mol. Biol. 19, 771-780.
17. Franzén, L.-G., Frank, G., Zuber, H. & Rochaix, J.-D. (1989a) Isolation and characterization of cDNA clones encoding the 17.9 and 8.1 kDa subunits of photosystem I from Chlamydomonas reinhardtii, Plant Mol. Biol. 12, 463-474.
18. Franzén, L.-G., Frank, G., Zuber, H. & Rochaix, J.-D. (1989b) Isolation and characterisation of cDNA clones encoding photosystem I subunits with molecular masses 11.0, 10.0 and 8.4 kDa from Chlamydomonas reinhardtii, Mol. & Gen. Genet. 219, 137-144.
19. Franzén, L.-G., Rochaix, J.-D. & von Heijne, G. (1990) Chloroplast transit peptides from the green alga Chlamydomonas reinhardtii share features with both mitochondrial and higher plant chloroplast presequences, FEBS Lett. 260, 165-168.
20. Genetics Computer Group (1994) Program manual for the Wisconsin package. Version 8. Wisconsin.
21. Giessler, A., Geier, B. M., di Rago, J.-P., Slonimski, P. P. & von Jagow, G. (1994) Analysis of cytochrome b amino acid residues forming the contact face with the iron-sulfur subunit of ubiquinol:cytochrome c reductase in Saccharomyces cerevisiae, Eur. J. Biochem. 222, 147-154.
22. Glick, B. S., Beasley, E. M. & Schatz, G. (1992) Protein sorting in mitochondria, Trends Biochem. Sci. 17, 453-459.
23. González-Halphen, D., Vásquez-Acevedo, M. & Garcia-Ponce, B. (1991) On the interaction of mitochondrial complex III with the Rieske iron-sulfur protein (subunit V), J. Biol. Chem. 266, 3870-3876.
24. 1 complex of iron-sulfur protein lacking the iron-sulfur cluster, J. Biol. Chem. 266, 22485-22492.
25. Harnisch, U., Weiss, H. & Sebald, W. (1985) The primary structure of the iron-sulfur subunit of ubiquinol-cytochrome c reductase from Neurospora, determined by cDNA and gene sequencing, Eur. J. Biochem. 149, 95-99.
26. Hartl, F.-U., Schmidt, B., Wachter, E., Weiss, H. & Neupert, W. (1986) Transport into mitochondria and intramitochondrial sorting of the Fe/S protein of the ubiquinol-cytochrome c reductase, Cell 47, 939-951.
27. Hartl, F.-U., Pfanner, N., Nicholoson, D. W. & Neupert, W. (1989) Mitochondrial protein import, Biochim. Biophys. Acta 988, 1-45.
28. 2+-binding protein: homology in its protein sequence with calmodulin and the yeast CDC31 gene product, J. Cell Biol. 107, 133-140.
29. Huang, J., Struck, F., Matzinger, D. F. & Levings, C. S. III (1991) Functional analysis in yeast of cDNA coding for the mitochondrial Rieske iron-sulfur protein of higher plants, Proc. Natl Acad. Sci. USA 88, 10716-10720.
30. Huang, J., Struck, F., Matzinger, D. F. & Levings, C. S. III (1994) Flower-enhanced expression of a nuclear-encoded mitochondrial respiratory protein is associated with changes in mitochondrion number, Plant Cell 6, 439-448.
31. Imbault, P., Wittemer, C., Johanningmeier, U., Jacobs, J. D. & Howell, S. H. (1988) Structure of the Chlamydomonas reinhardtii cabII-I gene encoding a chloropnyll-a/b-binding protein, Gene (Amst.) 73, 397-407.
32. Kallas, T., Spiller, S. & Malkin, R. (1988) Primary structure of co-transcribed genes encoding the Rieske Fe-S and cytochrome f proteins of the cyanobacterium Nostoc PCC 7906, Proc. Natl Acad. Sci. USA 85, 5794-5798.
33. Kitayama, M., Kitayama, K. & Togasaki, R. K. (1994) A cDNA clone encoding a ferredoxin-NADP+ reductase from Chlamydomonas reinhardtii, Plant Physiol. (Bethesda) 106, 1715-1716.
34. Kozak, M. (1991) Structural features in eukaryotic mRNAs that modulate the initiation of translation, J. Biol. Chem. 266, 19867-19870.
35. Kyte, J. & Doolittle, R. F. (1982) A simple method for displaying the hydropathic character of a protein, J. Mol. Biol. 157, 105-132.
36. Lancelin, J.-M., Bally, I., Arlaud, G. J., Blackledge, M., Gans, P., Stein, M. & Jacquot, J.-P. (1994) NMR structures of ferredoxin chloroplastic transit peptide from Chlamydomonas reinhardtii promoted by trifluoroethanol in aqueous solution, FEBS Lett. 343, 261-266.
37. 1 complex, Mol. & Gen. Genet. 224, 373-382.
38. Malkin, R. & Aparicio, P. J. (1975) Identification of a g = 1.90 high-potential iron-sulfur protein in chloroplasts, Biochem. Biophys. Res. Commun. 63, 1157-1160.
39. Matsudaira, P. (1987) Sequence from picomole quantitities of proteins electroblotted onto polyvinylidene difluoride membranes, J. Biol. Chem. 262, 10035-10037.
40. Mayfield, S. P., Rahire, M., Frank, G., Zuber, H. & Rochaix, J.-D. (1987) Expression of the nuclear gene encoding oxygen-evolving enhancer protein 2 is required for high levels of photosynthetic oxygen evolution in Chlamydomonas reinhardtii, Proc. Natl Acad. Sci. USA 84, 749-753.
41. Mayfield, S. P., Schirmer-Rahire, G., Frank, H., Zuber, H. & Rochaix, J.-D. (1989) Analysis of the genes of the OEE1 and OEE3 proteins of the photosystem II complex of Chlamydomonas reinhardtii, Plant Mol. Biol. 12, 683-693.
42. Merchant, S., Hill, K., Kim, J. H., Thompson, J., Zaitlin, D. & Bogorad, L. (1990) Isolation and characterization of a complementary DNA clone for an algal pre-apoplastocyanin, J. Biol. Chem. 265, 12372-12379.
43. 1 complex deduced from cDNA analysis, Biochem. Int. 20, 155-160.
44. Olive, J., Wollman, F.-A., Bennoun, P. & Recouvreur, M. (1981) Ultrastructure of thylakoid membranes in C. reinhardtii: evidence for variations in the partition coefficient of the light-harvesting complex-containing particles upon membrane fracture. Arch. Biochem. Biophys. 208, 456-467.
45. Piccioni, R. G., Bennoun, P. & Chua, N.-H. (1981) A nuclear mutant of Chlamydomonas reinhardtii defective in photosynthetic photophosphorylation. Characterization of the algal coupling factor ATPase, Eur. J. Biochem. 117, 93-102.
46. Rieske, J. S., Hansen, R. E. & Zaugg, W. S. (1964) Studies on the electron transfer system LVII. Properties of a new oxidation-reduction component ot the respiration chain as studied by electron paramagnetic resonance spectroscopy, J. Biol. Chem. 239, 3017-3021.
47. Roise, D., Horvath, S. J., Tomich, J. M., Richards, J. H. & Schatz, G. (1986) A chemically synthesized pro-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers, EMBO J. 5, 1327-1334.
48. 1 complex from beef heart, Methods Enzymol. 126, 224-237.
49. Schägger, H., Borchart, U., Machleidt, W., Link, T. A. & von Jagow, G. (1987) Isolation and amino acid sequence of the 'Rieske' iron sulfur protein of beef heart ubiquinol:cytochrome c reductase, FEBS Lett. 219, 161-168.
50. Sharpe, J. A. & Day, A. (1993) Structure, evolution and expression of the mitochondrial ADP/ATP translocator gene from Chlamydomonas reinhardtii, Mol. & Gen. Genet. 237, 134-144.
51. Silflow, C. D., Chisholm, R. L., Conner, T. W. & Ranum, L. P. W. (1985) The two alpha tubulin genes of Chlamydomonas reinhardtii code for slightly different proteins, Mol. Cell. Biol. 5, 2389-2398.
52. Stein, M., Jacquot, J.-P. & Miginiac-Maslow, M. (1993) A cDNA clone encoding Chlamydomonas reinhardtii preferredoxin, Plant Physiol. (Bethesda) 102, 1349-1350.
53. von Heijne, G. (1986) Mitochondrial targeting sequences may form amphiphilic helices, EMBO J. 5, 1335-1342.
54. von Heijne, G., Steppuhn, J. & Herrmann, R. G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides, Eur. J. Biochem. 180, 535-545.
55. von Heijne, G. (1990a) Protein targeting signals, Curr. Opin. Cell Biol. 2, 604-608.
56. von Heijne, G. (1990b) The signal peptide. J. Membr. Biol. 115, 195-201.
57. Yu, L. M. & Selman, B. R. (1988) cDNA sequence and predicted primary structure of the gamma subunit from the ATP synthase from Chlamydomonas reinhardtii, J. Biol. Chem. 263, 19342-19345.