The strictly aerobic yeast Yarrowia lipolytica tolerates loss of a mitochondrial DNA-packaging protein

Eukaryotic Cell

Volumn 13, Issue 9, 2014, Pages 1143-1157

  Bakkaiova, Jana ^a   Arata, Kosuke ^b   Matsunobu, Miki ^b   Ono, Bungo ^b   Aoki, Tomoyo ^b   Lajdova, Dana ^a   Nebohacova, Martina ^a   Nosek, Jozef ^a   Miyakawa, Isamu ^b   Tomaska, Lubomir ^a  

^a Physics and Informatics   (Slovakia)

^b YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

YARROWIA LIPOLYTICA;

ABF2 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; HIGH MOBILITY GROUP B PROTEIN; MITOCHONDRIAL DNA; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; GENE INACTIVATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRIAL GENOME; MITOCHONDRION; MUTATION; SACCHAROMYCES CEREVISIAE; YARROWIA;

AMINO ACID SEQUENCE; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; GENE KNOCKOUT TECHNIQUES; GENOME, MITOCHONDRIAL; HMGB PROTEINS; MITOCHONDRIA; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; YARROWIA;

EID: 84907470740     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00092-14     Document Type: Article

References (94)

1. Kaufman BA, Kolesar JE, Perlman PS, Butow RA. 2003. A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccharomyces cerevisiae. J. Cell Biol. 163:457-461. http://dx.doi.org/10.1083/jcb.200306132.
2. Miyakawa I, Aoi H, Sando N, Kuroiwa T. 1984. Fluorescence microscopic studies of mitochondrial nucleoids during meiosis and sporulation in the yeast, Saccharomyces cerevisiae. J. Cell Sci. 66:21-38.
3. Miyakawa I, Sando N, Kawano S, Nakamura S, Kuroiwa T. 1987. Isolation of morphologically intact mitochondrial nucleoids from the yeast, Saccharomyces cerevisiae. J. Cell Sci. 88:431-439.
4. Miyakawa I, Miyamoto M, Kuroiwa T, Sando N. 2004. DNA content of individual mitochondrial nucleoids varies depending on the culture conditions of the yeast Saccharomyces cerevisiae. Cytologia 69:101-107. http: //dx.doi.org/10.1508/cytologia.69.101.
5. Williamson DH, Fennell DJ. 1975. The use of fluorescent DNA-binding agent for detecting and separating yeast mitochondrial DNA. Methods Cell Biol. 12:335-351. http://dx.doi.org/10.1016/S0091-679X(08)60963-2.
6. Williamson DH, Fennell DJ. 1979. Visualization of yeast mitochondrial DNA with the fluorescent stain "DAPI." Methods Enzymol. 56:728-733.
7. Brown TA, Tkachuk AN, Shtengel G, Kopek BG, Bogenhagen DF, Hess HF, Clayton DA. 2011. Superresolution fluorescence imaging of mitochondrial nucleoids reveals their spatial range, limits, and membrane interaction. Mol. Cell. Biol. 31:4994-5010. http://dx.doi.org/10.1128/MCB. 05694-11.
8. Kukat C, Wurm CA, Spahr H, Falkenberg M, Larsson NG, Jakobs S. 2011. Super-resolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc. Natl. Acad. Sci. U. S. A. 108:13534-13539. http://dx.doi. org/10.1073/pnas.1109263108.
9. Copeland WC. 2012. Defects in mitochondrial DNA replication and human disease. Crit. Rev. Biochem. Mol. Biol. 47:64-74. http://dx.doi.org /10.3109/10409238.2011.632763.
10. Friedman JR, Nunnari J. 2014. Mitochondrial form and function. Nature 505:335-343. http://dx.doi.org/10.1038/nature12985.
11. Bogenhagen DF. 2011. Mitochondrial DNA nucleoid structure. Biochim. Biophys. Acta 1819:914-920. http://dx.doi.org/10.1016/j.bbagrm.2011. 11.005.
12. Chen XJ, Wang X, Kaufman BA, Butow RA. 2005. Aconitase couples metabolic regulation to mitochondrial DNA maintenance. Science 307: 714-717. http://dx.doi.org/10.1126/science.1106391.
13. Chen XJ, Butow RA. 2005. The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet. 6:815-825. http://dx.doi.org/10. 1038/nrg1708.
14. Kaufman BA, Newman SM, Hallberg RL, Slaughter CA, Perlman PS, Butow RA. 2000. In organello formaldehyde crosslinking of proteins to mtDNA: identification of bifunctional proteins. Proc. Natl. Acad. Sci. U. S. A. 97:7772-7777. http://dx.doi.org/10.1073/pnas.140063197.
15. Caron F, Jacq C, Rouviere-Yaniv J. 1979. Characterization of a histonelike protein extracted from yeast mitochondria. Proc. Natl. Acad. Sci. U. S. A. 76:4265-4269. http://dx.doi.org/10.1073/pnas.76.9.4265.
16. Certa U, Colavito-Shepanski M, Grunstein M. 1984. Yeast may not contain histone H1: the only known 'histone H1-like' protein in Saccharomyces cerevisiae is a mitochondrial protein. Nucleic Acids Res. 12:7975- 7985. http://dx.doi.org/10.1093/nar/12.21.7975.
17. Diffley JF, Stillman B. 1991. A close relative of the nuclear, chromosomal high-mobility group protein HMG1 in yeast mitochondria. Proc. Natl. Acad. Sci. U. S. A. 88:7864-7868. http://dx.doi.org/10.1073/pnas.88.17. 7864.
18. Diffley JF, Stillman B. 1992. DNA binding properties of an HMG1- related protein from yeast mitochondria. J. Biol. Chem. 267:3368-3374.
19. Friddle RW, Klare JE, Martin SS, Corzett M, Balhorn R, Baldwin EP, Baskin RJ, Noy A. 2004. Mechanism of DNA compaction by yeast mitochondrial protein Abf2p. Biophys. J. 86:1632-1639. http://dx.doi.org/10. 1016/S0006-3495(04)74231-9.
20. Kucej M, Kucejova B, Subramanian R, Chen XJ, Butow RA. 2008. Mitochondrial nucleoids undergo remodeling in response to metabolic cues. J. Cell Sci. 121:1861-1868. http://dx.doi.org/10.1242/jcs.028605.
21. Miyakawa I, Kanayama M, Fujita Y, Sato H. 2010. Morphology and protein composition of the mitochondrial nucleoids in yeast cells lacking Abf2p, a high mobility group protein. J. Gen. Appl. Microbiol. 56:455- 464. http://dx.doi.org/10.2323/jgam.56.455.
22. Newman SM, Zelenaya-Troitskaya O, Perlman PS, Butow RA. 1996. Analysis of mitochondrial DNA nucleoids in wild-type and a mutant strain of Saccharomyces cerevisiae that lacks the mitochondrial HMG box protein Abf2p. Nucleic Acids Res. 24:386-393. http://dx.doi.org/10.1093 /nar/24.2.386.
23. MacAlpine DM, Perlman PS, Butow RA. 1998. The high mobility group protein Abf2p influences the level of yeast mitochondrial DNA recombination intermediates in vivo. Proc. Natl. Acad. Sci. U. S. A. 95:6739-6743. http://dx.doi.org/10.1073/pnas.95.12.6739.
24. Zelenaya-Troitskaya O, Newman SM, Okamoto K, Perlman PS, Butow RA. 1998. Functions of the high mobility group protein, Abf2p, in mitochondrial DNA segregation, recombination and copy number in Saccharomyces cerevisiae. Genetics 148:1763-1776.
25. Okamoto K, Perlman PS, Butow RA. 1998. The sorting of mitochondrial DNA and mitochondrial proteins in zygotes: preferential transmission of mitochondrialDNAto the medial bud. J. Cell Biol. 142:613-623. http://dx. doi.org/10.1083/jcb.142.3.613.
26. Sia RA, Carrol S, Kalifa L, Hochmuth C, Sia EA. 2009. Loss of the mitochondrial nucleoid protein, Abf2p, destabilizes repetitive DNA in the yeast mitochondrial genome. Genetics 181:331-334. http://dx.doi.org/10. 1534/genetics.108.095786.
27. Zelenaya-Troitskaya O, Perlman PS, Butow RA. 1995. An enzyme in yeast mitochondria that catalyzes a step in branched-chain amino acid biosynthesis also functions in mitochondrial DNA stability. EMBO J. 14: 3268-3276.
28. Fisher RP, Clayton DA. 1985. A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy- and light-strand promoters dissected and reconstituted in vitro. J. Biol. Chem. 260:11330-11338.
29. Fisher RP, Clayton DA. 1988. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell. Biol. 8:3496-3509.
30. Parisi MA, Xu B, Clayton DA. 1993. A human mitochondrial transcriptional activator can functionally replace a yeast mitochondrial HMG-box protein both in vivo and in vitro. Mol. Cell. Biol. 13:1951-1961.
31. Yoon YG, Koob MD, Yoo YH. 2011. Mitochondrial genome-maintaining activity of mouse mitochondrial transcription factor A and its transcript isoform in Saccharomyces cerevisiae. Gene 484:52-60. http://dx.doi.org/10. 1016/j.gene.2011.05.032.
32. Parisi MA, Clayton DA. 1991. Similarity of human mitochondrial transcription factor 1 to high mobility group proteins. Science 252:965-969. http://dx.doi.org/10.1126/science.2035027.
33. Ngo HB, Kaiser JT, Chan DC. 2011. The mitochondrial transcription and packaging factor Tfam imposes a U-turn on mitochondrial DNA. Nat. Struct. Mol. Biol. 18:1290-1296. http://dx.doi.org/10.1038/nsmb.2159.
34. Rubio-Cosials A, Sidow JF, Jimenez-Menendez N, Fernandez-Millan P, Montoya J, Jacobs HT, Coll M, Bernado P, Sola M. 2011. Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter. Nat. Struct. Mol. Biol. 18:1281-1289. http://dx.doi. org/10.1038/nsmb.2160.
35. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. 1998. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat. Genet. 18:231-236. http://dx.doi.org/10.1038/ng0398-231.
36. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG. 2004. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum. Mol. Genet. 13:935-944. http://dx.doi.org/10.1093/hmg/ddh109.
37. Pohjoismaki JL, Wanrooij S, Hyvarinen AK, Goffart S, Holt IJ, Spelbrink JN, Jacobs HT. 2006. Alterations to the expression level of mitochondrial transcription factor A, TFAM, modify the mode of mitochondrial DNA replication in cultured human cells. Nucleic Acids Res. 34:5815-5828. http://dx.doi.org/10.1093/nar/gkl703.
38. Li H, Wang J, Wilhelmsson H, Hansson A, Thoren P, Duffy J, Rustin P, Larsson NG. 2000. Genetic modification of survival in tissue-specific knockout mice with mitochondrial cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 97:3467-3472. http://dx.doi.org/10.1073/pnas.97.7.3467.
39. Silva JP, Kohler M, Graff C, Oldfors A, Magnuson MA, Berggren PO, Larsson NG. 2000. Impaired insulin secretion and beta-cell loss in tissuespecific knockout mice with mitochondrial diabetes. Nat. Genet. 26:336- 340. http://dx.doi.org/10.1038/81649.
40. Sorensen L, Ekstrand M, Silva JP, Lindqvist E, Xu B, Rustin P, Olson L, Larsson NG. 2001. Late-onset corticohippocampal neurodepletion attributable to catastrophic failure of oxidative phosphorylation in MILON mice. J. Neurosci. 21:8082-8090.
41. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, Rustin P, Bruning JC, Kahn CR, Clayton DA, Barsh GS, Thoren P, Larsson NG. 1999. Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat. Genet. 21:133-137. http://dx.doi.org/10.1038/5089.
42. Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, Oldfors A, Westerblad H, Larsson NG. 2002. Increased mitochondrial mass in mitochondrial myopathy mice. Proc. Natl. Acad. Sci. U. S. A. 99:15066-15071. http://dx.doi.org/10.1073/pnas.232591499.
43. Dequard-Chablat M, Allandt C. 2002. Two copies of mthmg1, encoding a novel mitochondrial HMG-like protein, delay accumulation of mito- chondrialDNAdeletions in Podospora anserina. Eukaryot. Cell 1:503-513. http://dx.doi.org/10.1128/EC.1.4.503-513.2002.
44. Miyakawa I, Sato H, Maruyama Y, Nakaoka T. 2003. Isolation of the mitochondrial nucleoids from yeast Kluyveromyces lactis and analyses of the nucleoid proteins. J. Gen. Appl. Microbiol. 49:85-93. http://dx.doi.org /10.2323/jgam.49.85.
45. Miyakawa I, Yawata K. 2007. Purification of an Abf2p-like protein from mitochondrial nucleoids of yeast Pichia jadinii and its role in the packaging of mitochondrial DNA. Antonie Van Leeuwenhoek 91:197-207. http: //dx.doi.org/10.1007/s10482-006-9105-7.
46. Miyakawa I, Okamuro A, Kinsky S, Visacka K, Tomaska L, Nosek J. 2009. Mitochondrial nucleoids from the yeast Candida parapsilosis: expansion of the repertoire of proteins associated with mitochondrial DNA. Microbiology 155:1558-1568. http://dx.doi.org/10.1099/mic.0.027474-0.
47. Nosek J, Tomaska L, Bolotin-Fukuhara M, Miyakawa I. 2006. Mitochondrial chromosome structure: an insight from analysis of complete yeast genomes. FEMS Yeast Res. 6:356-370. http://dx.doi.org/10.1111/j. 1567-1364.2005.00016.x.
48. Sasaki N, Kuroiwa H, Nishitani C, Takano H, Higashiyama T, Kobayashi T, Shirai Y, Sakai A, Kawano S, Murakami-Murofushi K, Kuroiwa T. 2003. Glom is a novel mitochondrial DNA packaging protein in Physarum polycephalum and causes intense chromatin condensation without suppressing DNA functions. Mol. Biol. Cell 14:4758-4769. http: //dx.doi.org/10.1091/mbc.E03-02-0099.
49. Visacka K, Gerhold JM, Petrovicova J, Kinsky S, Joers P, Nosek J, Sedman J, Tomaska L. 2009. Novel subfamily of mitochondrialHMGbox-containing proteins: functional analysis of Gcf1p from Candida albicans. Microbiology 155:1226-1240. http://dx.doi.org/10.1099/mic.0.025759-0.
50. Itoh K, Izumi A, Mori T, Dohmae N, Yui R, Maeda-Sano K, Shirai Y, Kanaoka MM, Kuroiwa T, Higashiyama T, Sugita M, Murakami- Murofushi K, Kawano S, Sasaki N. 2011. DNA packaging proteins Glom and Glom2 coordinately organize the mitochondrial nucleoid of Physarum polycephalum. Mitochondrion 11:575-586. http://dx.doi.org/10. 1016/j.mito.2011.03.002.
51. Graser Y, Volovsek M, Arrington J, Schonian G, Presber W, Mitchell TG, Vilgalys R. 1996. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc. Natl. Acad. Sci. U. S. A. 93:12473-12477. http://dx.doi. org/10.1073/pnas.93.22.12473.
52. Casaregola S, Neuveglise C, Lepingle A, Bon E, Feynerol C, Artiguenave F, Wincker P, Gaillardin C. 2000. Genomic exploration of the hemiascomycetous yeasts: 17. Yarrowia lipolytica. FEBS Lett. 487:95-100. http: //dx.doi.org/10.1016/S0014-5793(00)02288-2.
53. Christen S, Sauer U. 2011. Intracellular characterization of aerobic glucose metabolism in seven yeast species by 13C flux analysis and metabolomics. FEMS Yeast Res. 11:263-272. http://dx.doi.org/10.1111/j.1567-1364. 2010.00713.x.
54. Chen DC, Beckerich JM, Gaillardin C. 1997. One-step transformation of the dimorphic yeast Yarrowia lipolytica. Appl. Microbiol. Biotechnol. 48: 232-235. http://dx.doi.org/10.1007/s002530051043.
55. Wang JH, Hung W, Tsai SH. 2011. High efficiency transformation by electroporation of Yarrowia lipolytica. J. Microbiol. 49:469-472. http://dx. doi.org/10.1007/s12275-011-0433-6.
56. Kerscher SJ, Okun JG, Brandt U. 1999. A single external enzyme confers alternative NADH:ubiquinone oxidoreductase activity in Yarrowia lipolytica. J. Cell Sci. 112:2347-2354.
57. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10. 1038/227680a0.
58. Kerscher SJ, Eschemann A, Okun PM, Brandt U. 2001. External alternative NADH:ubiquinone oxidoreductase redirected to the internal face of the mitochondrial inner membrane rescues complex I deficiency in Yarrowia lipolytica. J. Cell Sci. 114:3915-3921.
59. Nosek J, Fukuhara H. 1994. NADH dehydrogenase subunit genes in the mitochondrial DNA of yeasts. J. Bacteriol. 176:5622-5630.
60. Rycovska A, Valach M, Tomaska L, Bolotin-Fukuhara M, Nosek J. 2004. Linear versus circular mitochondrial genomes: intraspecies variability of mitochondrial genome architecture in Candida parapsilosis. Microbiology 150:1571-1580. http://dx.doi.org/10.1099/mic.0.26988-0.
61. Philippsen P, Stotz A, Scherf C. 1991. DNA of Saccharomyces cerevisiae. Methods Enzymol. 194:169 -182. http://dx.doi.org/10.1016/0076 -6879(91)94014-4.
62. Livak K. 1997. ABI Prism 7700 Sequence Detection System. User bulletin 2. PE Applied Biosystems, Foster City, CA.
63. Cross FR, Tinkelenberg AH. 1991. A potential positive feedback loop controllingCLN1andCLN2gene expression at the start of the yeast cell cycle. Cell 65:875-883. http://dx.doi.org/10.1016/0092-8674(91)90394-E.
64. Kroczek RA, Siebert E. 1990. Optimization of Northern analysis by vacuum- blotting, RNA-transfer visualization, and ultraviolet fixation. Anal. Biochem. 184:90-95. http://dx.doi.org/10.1016/0003-2697(90)90017-4.
65. Claros MG, Vincens P. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241: 779-786. http://dx.doi.org/10.1111/j.1432-1033.1996.00779.x.
66. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371. http://dx.doi. org/10.1038/nprot.2009.2.
67. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics /btm404.
68. Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963-972.
69. Tomaska L, Makhov AM, Nosek J, Kucejova B, Griffith JD. 2001. Electron microscopic analysis supports a dual role for the mitochondrial telomere-binding protein of Candida parapsilosis. J. Mol. Biol. 305:61-69. http://dx.doi.org/10.1006/jmbi.2000.4254.
70. Zickermann V, Bostina M, Hunte C, Ruiz T, Radermacher M, Brandt U. 2003. Functional implications from an unexpected position of the 49-kDa subunit of NADH:ubiquinone oxidoreductase. J. Biol. Chem. 278: 29072-29078. http://dx.doi.org/10.1074/jbc.M302713200.
71. Putrament A, Branowska H, Ejchart A, Prazmo W. 1975. Manganese mutagenesis in yeast. A practical application of manganese for the induction of mitochondrial antibiotic-resistant mutations. J. Gen. Microbiol. 90:265-270.
72. Kerscher S, Durstewitz G, Casaregola S, Gaillardin C, Brandt U. 2001. The complete mitochondrial genome of Yarrowia lipolytica. Comp. Funct. Genomics 2:80-90. http://dx.doi.org/10.1002/cfg.72.
73. Chang KJ, Lin G, Men LC, Wang CC. 2006. Redundancy of non-AUG initiators. A clever mechanism to enhance the efficiency of translation in yeast. J. Biol. Chem. 281:7775-7783. http://dx.doi.org/10.1074/jbc. M511265200.
74. Touriol C, Bornes S, Bonnal S, Audigier S, Prats H, Prats AC, Vagner S. 2003. Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol. Cell 95:169-178. http://dx.doi.org /10.1016/S0248-4900(03)00033-9.
75. Wach A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12:259-265.
76. Lawrence JJ, Daune M. 1976. Ethidium bromide as a probe of conformational heterogeneity of DNA in chromatin. The role of histone H1. Biochemistry 15:3301-3307.
77. Barnett JA, Payne RW, Yarrow D (ed). 2000. Yeasts: characteristics and identification. Cambridge University Press, Cambridge, United Kingdom.
78. Lehninger AL, Nelson DL, Cox MM (ed). 2005. Lehninger principles of biochemistry. W. H. Freeman, New York, NY.
79. Sebald W, Wachter E, Tzagoloff A. 1979. Identification of amino acid substitutions in the dicyclohexylcarbodiimide-binding subunit of the mitochondrial ATPase complex from oligomycin-resistant mutants of Saccharomyces cerevisiae. Eur. J. Biochem. 100:599-607. http://dx.doi.org/10. 1111/j.1432-1033.1979.tb04207.x.
80. Ooi BG, Novitski CE, Nagley P. 1985. DNA sequence analysis of the oli1 gene reveals amino acid changes in mitochondrial ATPase subunit 9 from oligomycin-resistant mutants of Saccharomyces cerevisiae. Eur. J. Biochem. 152:709 -714. http://dx.doi.org/10.1111/j.1432-1033.1985. tb09251.x.
81. 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. http://dx.doi.org/10.1016/0014-5793(86)80016-3.
82. Hedges SB, Blair JE, Venturi ML, Shoe JL. 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4:2. http://dx.doi.org/10.1186/1471-2148-4-2.
83. Barth G, Gaillardin C. 1997. Physiology and genetics of the dimorphic fungus Yarrowia lipolytica. FEMS Microbiol. Rev. 19:219-237. http://dx. doi.org/10.1111/j.1574-6976.1997.tb00299.x.
84. Kao LR, Megraw TL, Chae CB. 1993. Essential role of the HMG domain in the function of yeast mitochondrial histone HM: functional complementation ofHMby the nuclear nonhistone protein NHP6A. Proc. Natl. Acad. Sci. U. S. A. 90:5598-5602. http://dx.doi.org/10.1073/pnas.90.12.5598.
85. Gangelhoff TA, Mungalachetty PS, Nix JC, Churchill ME. 2009. Structural analysis and DNA binding of the HMG domains of the human mitochondrial transcription factor A. Nucleic Acids Res. 37:3153-3164. http: //dx.doi.org/10.1093/nar/gkp157.
86. Teng X, Dayhoff-Brannigan M, Cheng WC, Gilbert CE, Sing CN, Diny NL, Wheelan SJ, Dunham MJ, Boeke JD, Pineda FJ, Hardwick JM. 2013. Genome-wide consequences of deleting any single gene. Mol. Cell 52:485-494. http://dx.doi.org/10.1016/j.molcel.2013.09.026.
87. Kretzschmar A, Otto C, Holz M, Werner S, Hübner L, Barth G. 2013. Increased homologous integration frequency in Yarrowia lipolytica strains defective in non-homologous end-joining. Curr. Genet. 59:63-72. http: //dx.doi.org/10.1007/s00294-013-0389-7.
88. Baker MJ, Tatsuta T, Langer T. 2011. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol. 3:a007559. http://dx.doi. org/10.1101/cshperspect.a007559.
89. Herrmann JM, Woellhaf MW, Bonnefoy N. 2013. Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim. Biophys. Acta 1833:286-294. http://dx.doi.org/10.1016/j. bbamcr.2012.03.007.
90. Houtkooper RH, Mouchiroud L, Ryu D, Moullan N, Katsyuba E, Knott G, Williams RW, Auwerx J. 2013. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497:451-457. http://dx.doi.org /10.1038/nature12188.
91. Luzikov VN. 1999. Quality control: from molecules to organelles. FEBS Lett. 448:201-205. http://dx.doi.org/10.1016/S0014-5793(99)00344-0.
92. Li GW, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624 - 635. http://dx.doi.org/10.1016 /j.cell.2014.02.033.
93. Rak M, Tzagoloff A. 2009. F1-dependent translation of mitochondrially encoded Atp6p and Atp8p subunits of yeast ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 106:18509-18514. http://dx.doi.org/10.1073/pnas. 0910351106.
94. He J, Cooper HM, Reyes A, Di Re M, Sembongi H, Litwin TR, Gao J, Neuman KC, Fearnley IM, Spinazzola A, Walker JE, Holt IJ. 2012. Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res. 40:6109-6121. http://dx.doi.org/10. 1093/nar/gks266.