Atypical subunit composition of the chlorophycean mitochondrial F 1FO-ATP synthase and role of asa7 protein in stability and oligomycin resistance of the enzyme

Molecular Biology and Evolution

Volumn 27, Issue 7, 2010, Pages 1630-1644

  Lapaille, Marie ^a   Escobar Ramírez, Adelma ^b   Degand, Hervé ^c   Baurain, Denis ^a   Rodríguez Salinas, Elizabeth ^b   Coosemans, Nadine ^a   Boutry, Marc ^c   Gonzalez Halphen, Diego ^b   Remacle, Claire ^a   Cardol, Pierre ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Algae; Atypical subunits; Chlamydomonas; Enzyme evolution; Mitochondrial F1FO ATP synthase

Indexed keywords

ENZYME; OLIGOMYCIN; PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE ASSOCIATED 7 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; PROTEIN SUBUNIT; PROTON; SMALL INTERFERING RNA;

ALGAL GROWTH; ARTICLE; BIOENERGY; BREATHING; CHLOROPHYCEAE; CONTROLLED STUDY; DRUG RESISTANCE; IN VITRO STUDY; MITOCHONDRION; NONHUMAN; PRASINOPHYCEAE; PROTEIN STABILITY; RED ALGA; RNA INTERFERENCE; SCENEDESMUS; STREPTOPHYTA; TREBOUXIOPHYCEAE; ULVOPHYCEAE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; DIMERIZATION; ENZYMOLOGY; GENETICS; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; PHYLOGENY; PROTEIN SUBUNIT;

ALGAE; CHLAMYDOMONADALES; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; CHLOROCOCCALES; CHLOROCOCCUM ELLIPSOIDEUM; CHLOROPHYCEAE; CHLOROPHYTA; EMBRYOPHYTA; EUKARYOTA; MAMMALIA; PRASINOPHYCEAE; RHODOPHYTA; SCENEDESMUS OBLIQUUS; SPHAEROPLEALES; STREPTOPHYTA; TREBOUXIOPHYCEAE; ULVOPHYCEAE;

ADENOSINE TRIPHOSPHATE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; DIMERIZATION; DRUG RESISTANCE; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; OLIGOMYCINS; PHYLOGENY; PROTEIN SUBUNITS; PROTONS; RNA, SMALL INTERFERING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 77953741665     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq049     Document Type: Article

References (58)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Arnold I, Pfeiffer K, Neupert W, Stuart RA, Schagger H. 1998. Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. Embo J. 17:7170-7178.
3. Arselin G, Vaillier J, Salin B, Schaeffer J, Giraud MF, Dautant A, Brethes D, Velours J. 2004. The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology. J Biol Chem. 279:40392-40399.
4. Boyer PD. 2000. Catalytic site forms and controls in ATP synthase catalysis. Biochim Biophys Acta. 1458:252-262.
5. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248-254.
6. Brunner S, Everard-Gigot V, Stuart RA. 2002. Su e of the yeast F1Fo-ATP synthase forms homodimers. J Biol Chem. 277:48484-48489.
7. Bullerwell CE, Gray MW. 2004. Evolution of the mitochondrial genome: protist connections to animals, fungi and plants. Curr Opin Microbiol. 7:528-534.
8. Cardol P, González-Halphen D, Reyes-Prieto A, Baurain D, Matagne RF, Remacle C. 2005. The mitochondrial oxidative phosphorylation proteome of Chlamydomonas reinhardtii deduced from the Genome Sequencing Project. Plant Physiol. 137:447-459.
9. Cardol P, Lapaille M, Minet P, Matagne RF, Franck F, Remacle C. 2006. ND3 and ND4L subunits of mitochondrial complex I, both nucleus-encoded in Chlamydomonas reinhardtii, are required for the activity and assembly of the enzyme. Eukaryot Cell. 5:1460-1467.
10. Cardol P, Matagne RF, Remacle C. 2002. Impact of mutations affecting ND mitochondria-encoded subunits on the activity and assembly of complex I in Chlamydomonas. Implication for the structural organization of the enzyme. J Mol Biol. 319:1211-1221.
11. Cardol P, Vanrobaeys F, Devreese B, Van Beeumen J, Matagne R, Remacle C. 2004. Higher plant-like subunit composition of the mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes. Biochim Biophys Acta. 1658:212-224.
12. Debuchy R, Purton S, Rochaix JD. 1989. The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. Embo J. 8:2803-2809.
13. Derelle E, Ferraz C, Rombauts S, et al. (26 co-authors). 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA. 103:11647-11652.
14. Duby F, Matagne RF. 1999. Alteration of dark respiration and reduction of phototrophic growth in a mitochondrial DNA deletion mutant of Chlamydomonas lacking cob, nd4, and the 3# end of nd5. Plant Cell. 11:115-125.
15. Dudkina NV, Heinemeyer J, Keegstra W, Boekema EJ, Braun HP. 2005. Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett. 579:5769-5772.
16. Edgar RC. 2004. MUSCLE:amultiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 5:113.
17. Eriksson M, Gardestrom P, Samuelsson G. 1995. Isolation, purification and characterization of mitochondria from Chla-mydomonas reinhardtii. Plant Physiol. 107:479-483.
18. Gans P, Rebeille F. 1990. Control in the dark of the plastoquinone redox state by mitochondrial activity in Chlamydomonas reonhardtii. Biochim Biophys Acta. 1015:150-155.
19. Grigoras I, Lazard M, Plateau P, Blanquet S. 2008. Functional characterization of the Saccharomyces cerevisiae ABC-transporter Yor1p overexpressed in plasma membranes. Biochim Biophys Acta. 1778:68-78.
20. Harris EH. 1989. The Chlamydomonas sourcebook. San Diego (CA): Academic Press.
21. Heazlewood JL, Whelan J, Millar AH. 2003. The products of the mitochondrial orf25 and orfB genes are FO components in the plant F1FO ATP synthase. FEBS Lett. 540:201-205.
22. Hong S, Pedersen PL. 2008. ATP synthase and the actions of inhibitors utilized to study its roles in human health, disease, and other scientific areas. Microbiol Mol Biol Rev. 72:590-641.
23. John UP, Nagley P. 1986. Amino acid substitutions in mitochondrial ATPase subunit 6 of Saccharomyces cerevisiae leading to oligomycin resistance. FEBS Lett. 207:79-83. (Pubitemid 17179367)
24. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. 2008. NCBI BLAST: a better web interface. Nucleic Acids Res. 36:W5-W9.
25. Katzmann DJ, Hallstrom TC, Voet M, Wysock W, Golin J, Volckaert G, Moye-Rowley WS. 1995. Expression of an ATP-binding cassette transporter-encoding gene (YOR1) is required for oligomycin resistance in Saccharomyces cerevisiae. Mol Cell Biol. 15:6875-6883.
26. Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW. 2005. The tree of eukaryotes. Trends Ecol Evol. 20:670-676.
27. Kindle KL. 1990. High frequency nuclear transformation of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA. 87:1228-1232.
28. Lewis LA, McCourt RM. 2004. Green algae and the origin of land plants. Am J Bot. 91:1535-1556.
29. Marx S, Baumgartner M, Kannan S, Braun HP, Lang BF, Burger G. 2003. Structure of the bc1 complex from Seculamonas ecuadoriensis, a jakobid flagellate with an ancestral mitochon-drial genome. Mol Biol Evol. 20:145-153.
30. Minauro-Sanmiguel F, Wilkens S, Garcia JJ. 2005. Structure of dimeric mitochondrial ATP synthase: novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc Natl Acad Sci USA. 102:12356-12358.
31. Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D. 2009. Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. Plant J.
32. Müller T, Rahmann S, Dandekar T, Wolf M. 2004. Accurate and robust phylogeny estimation based on profile distances: a study of the Chlorophyceae (Chlorophyta). BMC Evol Biol. 4:20.
33. Nagley P, Hall RM, Ooi BG. 1986. Amino acid substitutions in mitochondrial ATPase subunit 9 of Saccharomyces cerevisiae leading to oligomycin or venturicidin resistance. FEBS Lett. 195:159-163. (Pubitemid 16048994)
34. Newman SM, Boynton JE, Gillham NW, Randolph-Anderson BL, Johnson AM, Harris EH. 1990. Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: molecular and genetic characterization of integration events. Genetics 126:875-888.
35. Ojaimi J, Pan J, Santra S, Snell WJ, Schon EA. 2002. An algal nucleus-encoded subunit of mitochondrial ATP synthase rescues a defect in the analogous human mitochondrial-encoded subunit. Mol Biol Cell. 13:3836-3844.
36. Peltier G, Thibault P. 1985. O(2) Uptake in the light in Chlamydomonas: evidence for persistent mitochondrial respiration. Plant Physiol. 79:225-230.
37. Pombert JF, Otis C, Lemieux C, Turmel M. 2004. The complete mitochondrial DNA sequence of the green alga Pseudendoclo-nium akinetum (Ulvophyceae) highlights distinctive evolutionary trends in the chlorophyta and suggests a sister-group relationship between the Ulvophyceae and Chlorophyceae. Mol Biol Evol. 21:922-935.
38. Pombert JF, Otis C, Lemieux C, Turmel M. 2005. The chloroplast genome sequence of the green alga Pseudendoclonium akinetum (Ulvophyceae) reveals unusual structural features and new insights into the branching order of chlorophyte lineages. Mol Biol Evol. 22:1903-1918.
39. Rak M, Zeng X, Briere JJ, Tzagoloff A. 2009. Assembly of F0 in Saccharomyces cerevisiae. Biochim Biophys Acta. 1793:108-116.
40. Remacle C, Baurain D, Cardol P, Matagne RF. 2001. Mutants of Chlamydomonas reinhardtii deficient in mitochondrial complex I. characterization of two mutations affecting the nd1 coding sequence. Genetics 158:1051-1060.
41. Remacle C, Cardol P, Coosemans N, Gaisne M, Bonnefoy N. 2006. High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc Natl Acad Sci USA. 103:4771-4776.
42. Rexroth S, Meyer zu Tittingdorf JM, Krause F, Dencher NA, Seelert H. 2003. Thylakoid membrane at altered metabolic state: challenging the forgotten realms of the proteome. Electropho-resis 24:2814-2823.
43. Rodriguez-Ezpeleta N, Philippe H, Brinkmann H, Becker B, Melkonian M. 2007. Phylogenetic analyses of nuclear, mitochon-drial, and plastid multigene data sets support the placement of Mesostigma in the Streptophyta. Mol Biol Evol. 24:723-731.
44. Schägger H, Von Jagow G. 1991. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem. 199:223-231.
45. Schroda M. 2006. RNA silencing in Chlamydomonas: mechanisms and tools. Curr Genet. 49:69-84.
46. Schwassmann HJ, Rexroth S, Seelert H, Dencher NA. 2007. Metabolism controls dimerization of the chloroplast FoF1 ATP synthase in Chlamydomonas reinhardtii. FEBS Lett. 581:1391-1396.
47. Turmel M, Lemieux C, Burger G, Lang BF, Otis C, Plante I, Gray MW. 1999. The complete mitochondrial DNA sequences of Neph-roselmis olivacea and Pedinomonas minor. Two radically different evolutionary patterns within green algae. Plant Cell. 11:1717-1730.
48. Van Lis R, Atteia A, Mendoza-Hernández G, González-Halphen D. 2003. Identification of novel mitochondrial protein components of Chlamydomonas reinhardtii. A proteomic approach. Plant Physiol. 132:318-330.
49. Van Lis R, Mendoza-Hernandez G, Groth G, Atteia A. 2007. New insights into the unique structure of the F0F1-ATP synthase from the chlamydomonad algae Polytomella sp. and Chlamy-domonas reinhardtii. Plant Physiol. 144:1190-1199.
50. Vázquez-Acevedo M, Cardol P, Cano-Estrada A, Lapaille M, Reyes-Prieto A, Remacle C, González-Halphen D. 2006. The mitochon-drial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stator-stalk and in the dimerization of the complex. J Bioenerg Biomembr. 38:271-282.
51. Velours J, Arselin G. 2000. The Saccharomyces cerevisiae ATP synthase. J Bioenerg Biomembr. 32:383-390.
52. Villavicencio-Queijeiro A, Vazquez-Acevedo M, Cano-Estrada A, et al. (12 co-authors). 2009. The fully-active and structurally-stable form of the mitochondrial ATP synthase of Polytomella sp. is dimeric. J Bioenerg Biomembr. 41:1-13.
53. Von Jagow G, Link TA. 1986. Use of specific inhibitors on the mitochondrial bc1 complex. Methods Enzymol. 126:253-271.
54. Walker JE, Dickson VK. 2006. The peripheral stalk of the mitochondrial ATP synthase. Biochim Biophys Acta. 1757:286-296.
55. 0-ATP synthase. FEBS Lett. 545:61-70.
56. Wittig I, Schagger H. 2008. Structural organization of mitochondrial ATP synthase. Biochim Biophys Acta. 1777:592-598.
57. Wittig I, Schagger H. 2009. Supramolecular organization of ATP synthase and respiratory chain in mitochondrial membranes. Biochim Biophys Acta. 1787:672-680.
58. Worden AZ, Lee JH, Mock T, et al. (51 co-authors). 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324: 268-272.