The mTERF protein MOC1 terminates mitochondrial DNA transcription in the unicellular green alga Chlamydomonas reinhardtii

Nucleic Acids Research

Volumn 41, Issue 13, 2013, Pages 6553-6567

  Wobbe, Lutz ^a   Nixon, Peter J ^b  

^a BIELEFELD UNIVERSITY   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION TERMINATION FACTOR; RIBOSOME RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ACCLIMATIZATION; ARTICLE; CHLAMYDOMONAS REINHARDTII; DNA DETERMINATION; DNA REPLICATION; DNA SEQUENCE; DNA TRANSCRIPTION; ENZYME ACTIVITY; GENE; GENETIC CODE; IN VITRO STUDY; MOC1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOTROPHY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTIST; TRANSCRIPTION TERMINATION;

AMINO ACID SEQUENCE; BINDING SITES; CHLAMYDOMONAS REINHARDTII; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; GENES, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; RNA, ANTISENSE; RNA, RIBOSOMAL; TRANSCRIPTION FACTORS; TRANSCRIPTION TERMINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84880549974     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt313     Document Type: Article

References (69)

1. Asin-Cayuela, J. and Gustafsson, C.M. (2007) Mitochondrial transcription and its regulation in mammalian cells. Trends Biochem. Sci., 32, 111-117. (Pubitemid 46389585)
2. Lipinski, K.A., Kaniak-Golik, A. and Golik, P. (2010) Maintenance and expression of the S. cerevisiae mitochondrial genome-from genetics to evolution and systems biology. Biochim. Biophys. Acta, 1797, 6-7.
3. Cardol, P., Gloire, G., Havaux, M., Remacle, C., Matagne, R. and Franck, F. (2003) Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol., 133, 2010-2020. (Pubitemid 38047327)
4. Vahrenholz, C., Riemen, G., Pratje, E., Dujon, B. and Michaelis, G. (1993) Mitochondrial DNA of Chlamydomonas reinhardtii: the structure of the ends of the linear 15.8-kb genome suggests mechanisms for DNA replication. Curr. Genet., 24, 241-247. (Pubitemid 23294055)
5. Smith, D.R. and Lee, R.W. (2008) Nucleotide diversity in the mitochondrial and nuclear compartments of Chlamydomonas reinhardtii: investigating the origins of genome architecture. BMC Evol. Biol., 8, 11.
6. Boer, P.H. and Gray, M.W. (1988) Scrambled ribosomal-RNA gene pieces in Chlamydomonas reinhardtii mitochondrial-DNA. Cell, 55, 399-411.
7. Vinogradova, E., Salinas, T., Cognat, V., Remacle, C. and Marechal-Drouard, L. (2009) Steady-state levels of imported tRNAs in Chlamydomonas mitochondria are correlated with both cytosolic and mitochondrial codon usages. Nucleic Acids Res., 37, 1521-1528.
8. Grant, D. and Chiang, K.S. (1980) Physical mapping and characterization of Chlamydomonas mitochondrial DNA molecules: their unique ends, sequence homogeneity, and conservation. Plasmid, 4, 82-96. (Pubitemid 11168399)
9. Ryan, R., Grant, D., Chiang, K.S. and Swift, H. (1978) Isolation and characterization of mitochondrial DNA from Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA, 75, 3268-3272. (Pubitemid 8389708)
10. Valach, M., Farkas, Z., Fricova, D., Kovac, J., Brejova, B., Vinar, T., Pfeiffer, I., Kucsera, J., Tomaska, L., Lang, B.F. et al. Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res., 39, 4202-4219.
11. Nosek, J., Tomaska, L., Fukuhara, H., Suyama, Y. and Kovac, L. (1998) Linear mitochondrial genomes: 30 years down the line. Trends Genet., 14, 184-188. (Pubitemid 28244242)
12. Boer, P.H. and Gray, M.W. (1986) The urf-5 gene of Chlamydomonas reinhardtii mitochondria - DNA-sequence and mode of transcription. EMBO J., 5, 21-28.
13. Gray, M.W. and Boer, P.H. (1988) Organization and expression of algal (Chlamydomonas reinhardtii) mitochondrial-DNA. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 319, 135-147.
14. Boer, P.H. and Gray, M.W. (1988) Genes encoding a subunit of respiratory nadh dehydrogenase (nd1) and a reverse transcriptase-like protein (rtl) are linked to ribosomal-RNA gene pieces in Chlamydomonas reinhardtii mitochondrial-DNA. EMBO J., 7, 3501-3508.
15. Duby, F., Cardol, P., Matagne, R.F. and Remacle, C. (2001) Structure of the telomeric ends of mtDNA, transcriptional analysis and complex I assembly in the dum24 mitochondrial mutant of Chlamydomonas reinhardtii. Mol. Genet. Genomics, 266, 109-114. (Pubitemid 32778669)
16. Barbrook, A.C., Howe, C.J., Kurniawan, D.P. and Tarr, S.J. (2010) Organization and expression of organellar genomes. Phil. Trans. R. Soc. B, 365, 785-797.
17. Liere, K., Weihe, A. and Borner, T. (2011) The transcription machineries of plant mitochondria and chloroplasts: Composition, function, and regulation. J. Plant Physiol., 168, 1345-1360.
18. Schonfeld, C., Wobbe, L., Borgstadt, R., Kienast, A., Nixon, P.J. and Kruse, O. (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J. Biol. Chem., 279, 50366-50374. (Pubitemid 39577854)
19. 2 production. PLoS One, 6, 15.
20. 2 production in engineered green algal cells. J. Biol. Chem., 280, 34170-34177. (Pubitemid 41443141)
21. Linder, T., Park, C.B., Asin-Cayuela, J., Pellegrini, M., Larsson, N.G., Falkenberg, M., Samuelsson, T. and Gustafsson, C.M. (2005) A family of putative transcription termination factors shared amongst metazoans and plants. Curr. Genet., 48, 265-269. (Pubitemid 41683415)
22. Kleine, T. (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front. Plant Sci., 3, 233.
23. Roberti, M., Polosa Paola, L., Bruni, F., Deceglie, S., Gadaleta Maria, N. and Cantatore, P. (2010) mTERF factors: a multifunction protein family. Biomol. Concepts, 1, 215.
24. Kruse, B., Narasimhan, N. and Attardi, G. (1989) Termination of transcription in human mitochondria: Identification and purification of a DNA binding protein factor that promotes termination. Cell, 58, 391-397. (Pubitemid 19191420)
25. Martin, M., Cho, J., Cesare, A.J., Griffith, J.D. and Attardi, G. (2005) Termination factor-mediated DNA loop between termination and initiation sites drives mitochondrial rRNA synthesis. Cell, 123, 1227-1240. (Pubitemid 41821781)
26. Park, C.B., Asin-Cayuela, J., Camara, Y., Shi, Y.H., Pellegrini, M., Gaspari, M., Wibom, R., Hultenby, K., Erdjument-Bromage, H., Tempst, P. et al. (2007) mTERF3 is a negative regulator of mammalian mtDNA transcription. Cell, 130, 273-285. (Pubitemid 47081137)
27. Wenz, T., Luca, C., Torraco, A. and Moraes, C.T. (2009) mTERF2 regulates oxidative phosphorylation by modulating mtDNA transcription. Cell Metab., 9, 499-511.
28. Hyvarinen, A.K., Kumanto, M.K., Marjavaara, S.K. and Jacobs, H.T. (2010) Effects on mitochondrial transcription of manipulating mTERF protein levels in cultured human HEK293 cells. BMC Mol. Biol., 11, 72.
29. Camara, Y., Asin-Cayuela, J., Park, C.B., Metodiev, M.B., Shi, Y.H., Ruzzenente, B., Kukat, C., Habermann, B., Wibom, R., Hultenby, K. et al. (2011) mTERF4 regulates translation by targeting the methyltransferase NSUN4 to the mammalian mitochondrial ribosome. Cell Metab., 13, 527-539.
30. Hyvarinen, A.K., Pohjoismaki, J.L., Reyes, A., Wanrooij, S., Yasukawa, T., Karhunen, P.J., Spelbrink, J.N., Holt, I.J. and Jacobs, H.T. (2007) The mitochondrial transcription termination factor mTERF modulates replication pausing in human mitochondrial DNA. Nucleic Acids Res., 35, 6458-6474. (Pubitemid 350111615)
31. Hyvarinen, A., Pohjoismaki, J., Holt, I. and Jacobs, H. (2011) Overexpression of mTERFD1 or mTERFD3 impairs the completion of mitochondrial DNA replication. Mol. Biol. Rep., 38, 1321-1328.
32. Fernandez-Silva, P., Martinez-Azorin, F., Micol, V. and Attardi, G. (1997) The human mitochondrial transcription termination factor (mTERF) is a multizipper protein but binds to DNA as a monomer, with evidence pointing to intramolecular leucine zipper interactions. EMBO J., 16, 1066-1079. (Pubitemid 27113185)
33. Roberti, M., Fernandez-Silva, P., Polosa, P.L., Fernandez-Vizarra, E., Bruni, F., Deceglie, S., Montoya, J., Gadaleta, M.N. and Cantatore, P. (2005) In vitro transcription termination activity of the Drosophila mitochondrial DNA-binding protein DmTTF. Biochem. Biophys. Res. Commun., 331, 357-362. (Pubitemid 40545184)
34. Roberti, M., Bruni, F., Polosa, P.L., Gadaleta, M.N. and Cantatore, P. (2006) The Drosophila termination factor DmTTF regulates in vivo mitochondrial transcription. Nucleic Acids Res., 34, 2109-2116. (Pubitemid 44314208)
35. Harris, E.H. (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego.
36. Asamizu, E., Nakamura, Y., Sato, S., Fukuzawa, H. and Tabata, S. (1999) A large scale structural analysis of cDNAs in a unicellular green Alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res., 6, 369-373. (Pubitemid 129705037)
37. Atteia, A., Adrait, A., Brugiere, S., Tardif, M., van Lis, R., Deusch, O., Dagan, T., Kuhn, L., Gontero, B., Martin, W. et al. (2009) A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor. Mol. Biol. Evol., 26, 1533-1548.
38. Chomczynski, P. and Sacchi, N. (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat. Protoc., 1, 581-585.
39. Murray, M.G. and Thompson, W.F. (1980) Rapid isolation of high molecular-weight plant DNA. Nucleic Acids Res., 8, 4321-4325.
40. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
41. Blackwell, T.K. (1995) Selection of protein-binding sites from random nucleic-acid sequences. Methods Enzymol., 254, 604-618.
42. Kosa, P., Valach, M., Tomaska, L., Wolfe, K.H. and Nosek, J. (2006) Complete DNA sequences of the mitochondrial genomes of the pathogenic yeasts Candida orthopsilosis and Candida metapsilosis: insight into the evolution of linear DNA genomes from mitochondrial telomere mutants. Nucleic Acids Res., 34, 2472-2481. (Pubitemid 43985685)
43. Tardif, M., Atteia, A., Specht, M., Cogne, G., Rolland, N., Brugiere, S., Hippler, M., Ferro, M., Bruley, C., Peltier, G. et al. (2012) PredAlgo, a new subcellular localization prediction tool dedicated to green algae. Mol. Biol. Evol., 26, 3625-3639.
44. Claros, M.G. and Vincens, P. (1996) Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem., 241, 779-786. (Pubitemid 26379380)
45. Alberts, B. and Herrick, G. (1971) DNA-cellulose chromatography. Methods Enzymol., 21, 198-217.
46. Wright, W.E., Binder, M. and Funk, W. (1991) Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol. Cell. Biol., 11, 4104-4110. (Pubitemid 21895800)
47. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res., 37, W202-W208.
48. Tracy, R.L. and Stern, D.B. (1995) Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr. Genet., 28, 205-216.
49. Temperley, R.J., Wydro, M., Lightowlers, R.N. and Chrzanowska- Lightowlers, Z.M. (2010) Human mitochondrial mRNAs-like members of all families, similar but different. Biochim. Biophys. Acta, 1797, 1081-1085.
50. Slomovic, S., Laufer, D., Geiger, D. and Schuster, G. (2005) Polyadenylation and degradation of human mitochondrial RNA: the prokaryotic past leaves its mark. Mol. Cell. Biol., 25, 6427-6435. (Pubitemid 41023219)
51. Mercer, T.R., Neph, S., Dinger, M.E., Crawford, J., Smith, M.A., Shearwood, A., Marie, J., Haugen, E., Bracken, C.P., Rackham, O. et al. (2011) The human mitochondrial transcriptome. Cell, 146, 645-658.
52. Ma, D.P., King, Y.T., Kim, Y., Luckett, W.S. Jr, Boyle, J.A. and Chang, Y.F. (1992) Amplification and characterization of an inverted repeat from the Chlamydomonas reinhardtii mitochondrial genome. Gene, 119, 253-257.
53. Yakubovskaya, E., Mejia, E., Byrnes, J., Hambardjieva, E. and Garcia-Diaz, M. (2010) Helix unwinding and base flipping enable human mTERF1 to terminate mitochondrial transcription. Cell, 141, 982-993.
54. Asin-Cayuela, J., Schwend, T., Farge, G. and Gustafsson, C.M. (2005) The human mitochondrial transcription termination factor (mTERF) is fully active in vitro in the nonphosphorylated form. J. Biol. Chem., 280, 25499-25505. (Pubitemid 40962254)
55. Rycovska, A., Valach, M., Tomaska, L., Bolotin-Fukuhara, M. and Nosek, J. (2004) Linear versus circular mitochondrial genomes: intraspecies variability of mitochondrial genome architecture in Candida parapsilosis. Microbiology, 150, 1571-1580. (Pubitemid 38744757)
56. Tomaska, L., Nosek, J., Kramara, J. and Griffith, J.D. (2009) Telomeric circles: universal players in telomere maintenance? Nat. Struct. Mol. Biol., 16, 1010-1015.
57. Tomaska, L., Makhov, A.M., Griffith, J.D. and Nosek, J. (2002) t-loops in yeast mitochondria. Mitochondrion, 1, 455-459. (Pubitemid 34461244)
58. de Lange, T. (2009) How telomeres solve the end-protection problem. Science, 326, 948-952.
59. Rorbach, J. and Minczuk, M. (2012) The post-transcriptional life of mammalian mitochondrial RNA. Biochem. J., 444, 357-373.
60. Holec, S., Lange, H., Kuhn, K., Alioua, M., Borner, T. and Gagliardi, D. (2006) Relaxed transcription in Arabidopsis mitochondria is counterbalanced by RNA stability control mediated by polyadenylation and polynucleotide phosphorylase. Mol. Cell. Biol., 26, 2869-2876.
61. Sharwood, R.E., Halpert, M., Luro, S., Schuster, G. and Stern, D.B. (2011) Chloroplast RNase J compensates for inefficient transcription termination by removal of antisense RNA. RNA, 17, 2165-2176.
62. Robles, P., Micol, J.L. and Quesada, V. (2012) Arabidopsis MDA1, a nuclear-encoded protein, functions in chloroplast development and abiotic stress responses. PLoS One, 7, 14.
63. Babiychuk, E., Vandepoele, K., Wissing, J., Garcia-Diaz, M., De Rycke, R., Akbari, H., Joubes, J., Beeckman, T., Jansch, L., Frentzen, M. et al. (2011) Plastid gene expression and plant development require a plastidic protein of the mitochondrial transcription termination factor family. Proc. Natl Acad. Sci. USA, 108, 6674-6679.
64. 2-induced cell death. Plant J., 60, 399-410.
65. Quesada, V., Sarmiento-Manus, R., Gonzalez-Bayon, R., Hricova, A., Perez-Marcos, R., Gracia-Martinez, E., Medina-Ruiz, L., Leyva-Diaz, E., Ponce, M.R. and Micol, J.L. (2011) Arabidopsis RUGOSA2 encodes an mTERF family member required for mitochondrion, chloroplast and leaf development. Plant J., 68, 738-753.
66. Kim, M., Lee, U., Small, I., des Francs-Small, C.C. and Vierling, E. (2012) Mutations in an Arabidopsis mitochondrial transcription termination factor-related protein enhance thermotolerance in the absence of the major molecular chaperone HSP101. Plant Cell, 24, 3349-3365.
67. Pfalz, J., Liere, K., Kandlbinder, A., Dietz, K.J. and Oelmuller, R. (2006) PTAC2,-6, and-12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell, 18, 176-197. (Pubitemid 43951323)
68. Majeran, W., Friso, G., Asakura, Y., Qu, X., Huang, M., Ponnala, L., Watkins, K.P., Barkan, A. and van Wijk, K.J. (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol., 158, 156-189.
69. Pesaresi, P., Masiero, S., Eubel, H., Braun, H.P., Bhushan, S., Glaser, E., Salamini, F. and Leister, D. (2006) Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell, 18, 970-991. (Pubitemid 43956148)