Mitochondrial DNA: More than an evolutionary bystander

Functional Ecology

Volumn 28, Issue 1, 2014, Pages 218-231

  Ballard, J William O ^a   Pichaud, Nicolas ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

Author keywords

Bioenergetics; Life history trade off; Mitochondrial function; OXPHOS

Indexed keywords

AGE CLASS; ANIMAL; BIOENERGETICS; EVOLUTIONARY BIOLOGY; FITNESS; LIFE HISTORY TRAIT; MITOCHONDRIAL DNA; MUTATION; TRADE-OFF;

ANIMALIA;

EID: 84892895007     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12177     Document Type: Review

References (159)

1. Achilli, A., Olivieri, A., Pala, M., Hooshiar Kashani, B., Carossa, V., Perego, U.A. et al. (2011) Mitochondrial DNA backgrounds might modulate diabetes complications rather than T2DM as a whole. PLoS One, 6, e21029.
2. Anderson, R. & Prolla, T. (2009) PGC-1alpha in aging and anti-aging interventions. Biochimica et Biophysica Acta, 1790, 1059-1066.
3. Aw, W.C., Correa, C.C., Clancy, D.J. & Ballard, J.W.O. (2011) Mitochondrial DNA variants in Drosophila melanogaster are expressed at the level of the organismal phenotype. Mitochondrion, 11, 756-763.
4. Ballard, J.W.O. & Melvin, R.G. (2011) Early life benefits and later life costs of a two amino acid deletion in Drosophila simulans. Evolution, 65, 1400-1412.
5. Ballard, J.W.O. & Whitlock, M.C. (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729-744.
6. Ballard, J.W.O., Melvin, R.G., Katewa, S.D. & Maas, K. (2007) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution, 61, 1735-1747.
7. Ballard, J.W.O., Melvin, R.G., Lazarou, M., Clissold, F.J. & Simpson, S.J. (2010) Cost of a naturally occurring two-amino acid deletion in cytochrome c oxidase subunit 7A in Drosophila simulans. The American Naturalist, 176, E98-E108.
8. Balloux, F., Handley, L.J., Jombart, T., Liu, H. & Manica, A. (2009) Climate shaped the worldwide distribution of human mitochondrial DNA sequence variation. Proceedings. Biological Sciences/The Royal Society, 276, 3447-3455.
9. Bandy, B. & Davison, A.J. (1990) Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radical Biology & Medicine, 8, 523-539.
10. Barreto, F.S. & Burton, R.S. (2013) Elevated oxidative damage is correlated with reduced fitness in interpopulation hybrids of a marine copepod. Proceedings of the Royal Society: Biological Science, 280, 20131521.
11. Battersby, B.J. & Shoubridge, E.A. (2001) Selection of a mtDNA sequence variant in hepatocytes of heteroplasmic mice is not due to differences in respiratory chain function or efficiency of replication. Human Molecular Genetics, 10, 2469-2479.
12. Bazin, E., Glemin, S. & Galtier, N. (2006) Population size does not influence mitochondrial genetic diversity in animals. Science, 312, 570-572.
13. Bellizzi, D., D'Aquila, P., Giordano, M., Montesanto, A. & Passarino, G. (2012) Global DNA methylation levels are modulated by mitochondrial DNA variants. Epigenomics, 4, 17-27.
14. Bernatchez, L., Glemet, H., Wilson, C.C. & Danzmann, R.G. (1995) Introgression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Canadian Journal of Fisheries and Aquatic Science, 52, 179-185.
15. Bird, A.P. & Taggart, M.H. (1980) Variable patterns of total DNA and rDNA methylation in animals. Nucleic Acids Research, 8, 1485-1497.
16. Blier, P.U., Dufresne, F. & Burton, R.S. (2001) Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. TRENDS in Genetics, 17(40), 0-406.
17. Brown, K.H., Lee, R.W. & Thorgaard, G.H. (2006) Use of androgenesis for estimating maternal and mitochondrial genome effects on development and oxygen consumption in rainbow trout, Oncorhynchus mykiss. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology, 143, 415-421.
18. Cannon, M.V., Dunn, D.A., Irwin, M.H., Brooks, A.I., Bartol, F.F., Trounce, I.A. et al. (2011) Xenomitochondrial mice: investigation into mitochondrial compensatory mechanisms. Mitochondrion, 11, 33-39.
19. Celotto, A.M., Chiu, W.K., Van Voorhies, W. & Palladino, M.J. (2011) Modes of metabolic compensation during mitochondrial disease using the Drosophila model of ATP6 dysfunction. PLoS One, 6, e25823.
20. Clancy, D.J. (2008) Variation in mitochondrial genotype has substantial lifespan effects which may be modulated by nuclear background. Aging Cell, 7, 795-804.
21. Clark, I.E., Dodson, M.W., Jiang, C., Cao, J.H., Huh, J.R., Seol, J.H. et al. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature, 441, 1162-1166.
22. Correa, C.C., Aw, W.C., Melvin, R.G., Pichaud, N. & Ballard, J.W. (2012) Mitochondrial DNA variants influence mitochondrial bioenergetics in Drosophila melanogaster. Mitochondrion, 12, 459-464.
23. Cunningham, J.T., Rodgers, J.T., Arlow, D.H., Vazquez, F., Mootha, V.K. & Puigserver, P. (2007) mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature, 450, 736-740.
24. De Benedictis, G., Rose, G., Carrieri, G., De Luca, M., Falcone, E., Passarino, G. et al. (1999) Mitochondrial DNA inherited variants are associated with successful aging and longevity in humans. Federation of American Societies for Experimental Biology journal, 13, 1532-1536.
25. Doan, J.W., Schmidt, T.R., Wildman, D.E., Uddin, M., Goldberg, A., Huttemann, M. et al. (2004) Coadaptive evolution in cytochrome c oxidase: 9 of 13 subunits show accelerated rates of nonsynonymous substitution in anthropoid primates. Molecular Phylogenetics and Evolution, 33, 944-950.
26. Doi, A., Suzuki, H. & Matsuura, E.T. (1999) Genetic analysis of temperature-dependent transmission of mitochondrial DNA in Drosophila. Heredity (Edinb), 82 (Pt 5), 555-560.
27. Dowling, D.K. & Simmons, L.W. (2009) Reactive oxygen species as universal constraints in life-history evolution. Proceedings of the Royal Society: Biological Science, 276, 1737-1745.
28. Drovetski, S.V., Kitaysky, A.S., Mode, N.A., Zink, R.M., Iqbal, U. & Barger, C. (2012) mtDNA haplotypes differ in their probability of being eliminated by a mass die-off in an abundant seabird. Heredity (Edinb), 109, 29-33.
29. Dunbar, D.R., Moonie, P.A., Jacobs, H.T. & Holt, I.J. (1995) Different cellular backgrounds confer a marked advantage to either mutant or wild-type mitochondrial genomes. Proceedings of the National Academy of Science of the United States of America, 92, 6562-6566.
30. Edmands, S. & Burton, R.S. (1999) Cytochrome C oxidase activity in interpopulation hybrids of a marine copepod: a test for nuclear-nuclear or nuclear-cytoplasmic coadaptation. Evolution, 53, 1972-1978.
31. Elena, S.F. & Sanjuán, R. (2003) Climb every mountain? Science, 302, 2074-2075.
32. Elson, J.L., Turnbull, D.M. & Howell, N. (2004) Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. American Journal of Human Genetics, 74, 229-238.
33. Fan, W., Waymire, K.G., Narula, N., Li, P., Rocher, C., Coskun, P.E. et al. (2008) A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science, 319, 958-962.
34. Feldhaus, P., Fraga, D.B., Ghedim, F.V., De Luca, R.D., Bruna, T.D., Heluany, M. et al. (2011) Evaluation of respiratory chain activity in lymphocytes of patients with Alzheimer disease. Metabolic Brain Disease, 26, 229-236.
35. Finkel, T. (1998) Oxygen radicals and signaling. Current Opinion in Cell Biology, 10, 248-253.
36. da Fonseca, R.R., Johnson, W.E., O'Brien, S.J., Ramos, M.J. & Antunes, A. (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics, 9, 119.
37. Frank, S.A. & Hurst, L.D. (1996) Mitochondria and male disease. Nature, 383, 224.
38. Freije, W.A., Mandal, S. & Banerjee, U. (2012) Expression profiling of attenuated mitochondrial function identifies retrograde signals in Drosophila. G3 : Genes - Genomes - Genetics, 2, 843-851.
39. Garvin, M.R., Bielawski, J.P. & Gharrett, A.J. (2011) Positive Darwinian selection in the piston that powers proton pumps in complex I of the mitochondria of Pacific salmon. PLoS One, 6, e24127.
40. Gemmell, N.J., Metcalf, V.J. & Allendorf, F.W. (2004) Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends in Ecology & Evolution, 19, 238-244.
41. Gershman, B., Puig, O., Hang, L., Peitzsch, R.M., Tatar, M. & Garofalo, R.S. (2007) High-resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiological Genomics, 29, 24-34.
42. Gershoni, M., Templeton, A.R. & Mishmar, D. (2009) Mitochondrial bioenergetics as a major motive force of speciation. BioEssays, 31, 642-650.
43. Gil Borlado, M.C., Moreno Lastres, D., Gonzalez Hoyuela, M., Moran, M., Blazquez, A., Pello, R. et al. (2010) Impact of the mitochondrial genetic background in complex III deficiency. PLoS One, 5, e12801.
44. Gillespie, J.H. (2000) Genetic drift in an infinite population. The pseudohitchhiking model. Genetics, 155, 909-919.
45. Grewal, S.S. (2009) Insulin/TOR signaling in growth and homeostasis: a view from the fly world. The International Journal of Biochemistry & Cell Biology, 41, 1006-1010.
46. Grossman, L.I., Wildman, D.E., Schmidt, T.R. & Goodman, M. (2004) Accelerated evolution of the electron transport chain in anthropoid primates. Trends in Genetics, 20, 578-585.
47. Guertin, D.A., Guntur, K.V., Bell, G.W., Thoreen, C.C. & Sabatini, D.M. (2006) Functional genomics identifies TOR-regulated genes that control growth and division. Current Biology, 16, 958-970.
48. Handschin, C. & Spiegelman, B.M. (2008) The role of exercise and PGC1alpha in inflammation and chronic disease. Nature, 454, 463-469.
49. Hauswirth, W.W. & Laipis, P.J. (1982) Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proceedings of the National Academy of Sciences of the United States of America, 79, 4686-4690.
50. Heckmann, L.H., Sibly, R.M., Connon, R., Hooper, H.L., Hutchinson, T.H., Maund, S.J. et al. (2008) Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biology, 9, R40.
51. Herrera, C.M. & Bazaga, P. (2011) Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Molecular Ecology, 20, 1675-1688.
52. Horan, M.P., Gemmell, N.J. & Wolff, J.N. (2013a) From evolutionary bystander to master manipulator: the emerging roles for the mitochondrial genome as a modulator of nuclear gene expression. European Journal of Human Genetics. doi: 10.1038/ejhg.2013.75.
53. Horan, M.P., Pichaud, N. & Ballard, J.W.O. (2012) Review: quantifying mitochondrial dysfunction in complex diseases of aging. Journal of Gerontology: Biological Sciences, 67, 1022-1035.
54. Horan, M.P., Rumbley, J.N., Melvin, R.G., Le Couteur, D.G. & Ballard, J.W.O. (2013b) Quaternary protein modeling to predict the function of DNA variation found in human mitochondrial cytochrome c oxidase. Journal of Human Genetics, 58, 127-134.
55. Houten, S.M. & Auwerx, J. (2004) PGC-1alpha: turbocharging mitochondria. Cell, 119, 5-7.
56. Hudson, G., Nalls, M., Evans, J.R., Breen, D.P., Winder-Rhodes, S., Morrison, K.E. et al. (2013) Two-stage association study and meta-analysis of mitochondrial DNA variants in Parkinson disease. Neurology, 80, 2042-2048.
57. Huey, R.B. & Berrigan, D. (2001) Temperature, demography, and ectotherm fitness. The American Naturalist, 158, 204-210.
58. Huttemann, M., Lee, I., Pecinova, A., Pecina, P., Przyklenk, K. & Doan, J.W. (2008) Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. Journal of Bioenergetics and Biomembranes, 40, 445-456.
59. Hwang, S., Kwak, S.H., Bhak, J., Kang, H.S., Lee, Y.R., Koo, B.K. et al. (2011) Gene expression pattern in transmitochondrial cytoplasmic hybrid cells harboring type 2 diabetes-associated mitochondrial DNA haplogroups. PLoS One, 6, e22116.
60. Innocenti, P., Morrow, E.H. & Dowling, D.K. (2011) Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science, 332, 845-848.
61. Inoue, K., Ogonuki, N., Yamamoto, Y., Takano, K., Miki, H., Mochida, K. et al. (2004) Tissue-specific distribution of donor mitochondrial DNA in cloned mice produced by somatic cell nuclear transfer. Genesis : The Journal Of Genetics And Development, 39, 79-83.
62. Jenuth, J.P., Peterson, A.C. & Shoubridge, E.A. (1997) Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nature Genetics, 16, 93-95.
63. Kao, L.P., Ovchinnikov, D. & Wolvetang, E. (2012) The effect of ethidium bromide and chloramphenicol on mitochondrial biogenesis in primary human fibroblasts. Toxicology and Applied Pharmacology, 261, 42-49.
64. Katewa, S.D. & Ballard, J.W.O. (2007) Sympatric Drosophila simulans flies with distinct mtDNA show difference in mitochondrial respiration and electron transport. Insect Biochemistry and Molecular Biology, 37, 213-222.
65. Kelly, R.D., Mahmud, A., McKenzie, M., Trounce, I.A. & St John, J.C. (2012) Mitochondrial DNA copy number is regulated in a tissue specific manner by DNA methylation of the nuclear-encoded DNA polymerase gamma A. Nucleic Acids Research, 40, 10124-10138.
66. Kim, I., Rodriguez-Enriquez, S. & Lemasters, J.J. (2007) Selective degradation of mitochondria by mitophagy. Archives of Biochemistry and Biophysics, 462, 245-253.
67. Kucharski, R., Maleszka, J., Foret, S. & Maleszka, R. (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science, 319, 1827-1830.
68. de Lamirande, E. & Gagnon, C. (1995) Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Human Reproduction, 10, 15-21.
69. Larsson, N.G. (2010) Somatic mitochondrial DNA mutations in mammalian aging. Annual Review of Biochemistry, 79, 683-706.
70. Lee, C., Yen, K. & Cohen, P. (2013) Humanin: a harbinger of mitochondrial-derived peptides? Trends in Endocrinology and Metabolism, 24, 222-228.
71. Lee, C.M., Chung, S.S., Kaczkowski, J.M., Weindruch, R. & Aiken, J.M. (1993) Multiple mitochondrial DNA deletions associated with age in skeletal muscle of rhesus monkeys. Journal of Gerontology, 48, B201-B205.
72. Lee, K.P., Simpson, S.J., Clissold, F.J., Brooks, R., Ballard, J.W.O., Taylor, P.W. et al. (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Sciences of the United States of America, 105, 2498-2503.
73. Linnane, A.W., Marzuki, S., Ozawa, T. & Tanaka, M. (1989) Mitochondrial DNA mutations as an important contributor to ageing and degenerative diseases. Lancet, 1, 642-645.
74. Liu, Z. & Butow, R.A. (1999) A transcriptional switch in the expression of yeast tricarboxylic acid cycle genes in response to a reduction or loss of respiratory function. Molecular and Cellular Biology, 19, 6720-6728.
75. Lucas, M.D., Drew, R.E., Wheeler, P.A., Verrell, P.A. & Thorgaard, G.H. (2004) Behavioral differences among rainbow trout clonal lines. Behavior Genetics, 34, 355-365.
76. Marden, J.H., Rogina, B., Montooth, K.L. & Helfand, S.L. (2003) Conditional tradeoff's between aging and organismal performance of Indy long-lived mutant flies. Proceedings of the National Academy of Science of the United States of America, 100, 3369-3373.
77. Matsuura, E.T., Niki, Y. & Chigusa, S.I. (1991) Selective transmission of mitochondrial DNA in heteroplasmic lines for intra- and interspecific combinations in Drosophila melanogaster. Japan Journal of Genetics, 66, 197-207.
78. Meiklejohn, C.D., Montooth, K.L. & Rand, D.M. (2007) Positive and negative selection on the mitochondrial genome. Trends in Genetics, 23, 259-263.
79. Melov, S., Hertz, G.Z., Stormo, G.D. & Johnson, T.E. (1994) Detection of deletions in the mitochondrial genome of Caenorhabditis elegans. Nucleic Acids Research, 22, 1075-1078.
80. Michikawa, Y., Mazzucchelli, F., Bresolin, N., Scarlato, G. & Attardi, G. (1999) Aging-dependent large accumulation of point mutations in the human mtDNA control region for replication. Science, 286, 774-779.
81. Miller, W., Schuster, S.C., Welch, A.J., Ratan, A., Bedoya-Reina, O.C., Zhao, F. et al. (2012) Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change. Proceedings of the National Academy of Sciences of the United States of America, 109, E2382-E2390.
82. Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A.G., Hosseini, S. et al. (2003) Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences of the United States of America, 100, 171-176.
83. Mishmar, D., Ruiz-Pesini, E., Mondragon-Palomino, M., Procaccio, V., Gaut, B. & Wallace, D.C. (2006) Adaptive selection of mitochondrial complex I subunits during primate radiation. Gene, 378, 11-18.
84. Moreno-Loshuertos, R., Acin-Perez, R., Fernandez-Silva, P., Movilla, N., Perez-Martos, A., Rodriguez de Cordoba, S. et al. (2006) Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nature Genetics, 38, 1261-1268.
85. Morton, N.E., Crow, J.F. & Muller, H.J. (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proceedings of the National Academy of Science of the United States of America, 42, 855-863.
86. Neiman, M. & Taylor, D.R. (2009) The causes of mutation accumulation in mitochondrial genomes. Proceedings. Biological Sciences/The Royal Society, 276, 1201-1209.
87. Nogales-Gadea, G., Pinos, T., Ruiz, J.R., Marzo, P.F., Fiuza-Luces, C., Lopez-Gallardo, E. et al. (2011) Are mitochondrial haplogroups associated with elite athletic status? A study on a Spanish cohort Mitochondrion, 11, 905-908.
88. Nord, A. & Nilsson, J.Å. (2011) Incubation temperature affects growth and energy metabolism in blue tit nestlings. American Naturalist, 178, 639-651.
89. Norrbom, J., Sundberg, C.J., Ameln, H., Kraus, W.E., Jansson, E. & Gustafsson, T. (2004) PGC-1alpha mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. Journal of Applied Physiology, 96, 189-194.
90. O'Hagan, H.M., Wang, W., Sen, S., Destefano Shields, C., Lee, S.S., Zhang, Y.W. et al. (2011) Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell, 20, 606-619.
91. Olivo, P.D., Van de Walle, M.J., Laipis, P.J. & Hauswirth, W.W. (1983) Nucleotide sequence evidence for rapid genotypic shifts in the bovine mitochondrial DNA D-loop. Nature, 306, 400-402.
92. Pennisi, E. (2000) Aging research. Old flies may hold secrets of aging. Science, 290, 2048.
93. Piatt, J.F. & Van Pelt, T.I. (1997) Mass-mortality of guillemots (Uria aalge) in the Gulf of Alaska in 1993. Marine Pollution Bulletin, 34, 656-662.
94. Pichaud, N., Chatelain, E.H., Ballard, J.W.O., Tanguay, R., Morrow, G. & Blier, P.U. (2010) Thermal sensitivity of mitochondrial metabolism in two distinct mitotypes of Drosophila simulans: evaluation of mitochondrial plasticity. Journal of Experimental Biology, 213, 1665-1675.
95. Pichaud, N., Ballard, J.W.O., Tanguay, R.M. & Blier, P.U. (2011) Thermal sensitivity of mitochondrial functions in permeabilized muscle fibers from two populations of Drosophila simulans with divergent mitotypes. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 301, R48-R59.
96. Pichaud, N., Ballard, J.W.O., Tanguay, R.M. & Blier, P.U. (2012) Naturally occurring mitochondrial DNA haplotypes exhibit metabolic differences: insight into functional properties of mitochondria. Evolution, 66, 3189-3197.
97. Pichaud, N., Ballard, J.W.O., Tanguay, R.M. & Blier, P.U. (2013a) Mitochondrial haplotype divergences affect specific temperature sensitivity of mitochondrial respiration. Journal of Bioenergetics and Biomembranes, 45, 25-35.
98. Pichaud, N., Messmer, M., Corea, C.C. & Ballard, J.W.O. (2013b) Diet influences the intake target and mitochondrial functions of Drosophila melanogaster males. Mitochondrion. doi: 10.1016/j.mito.2013.05.008
99. Pierron, D., Rocher, C., Amati-Bonneau, P., Reynier, P., Martin-Negrier, M.L., Allouche, S. et al. (2008) New evidence of a mitochondrial genetic background paradox: impact of the J haplogroup on the A3243G mutation. BMC Medical Genetics, 9, 41.
100. Piganeau, G. & Eyre-Walker, A. (2009) Evidence for variation in the effective population size of animal mitochondrial DNA. PLoS One, 4, e4396.
101. Polak, P. & Hall, M.N. (2009) mTOR and the control of whole body metabolism. Current Opinion in Cell Biology, 21, 209-218.
102. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M. & Spiegelman, B.M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 92, 829-839.
103. Qian, L., Song, X., Ren, H., Gong, J. & Cheng, S. (2004) Mitochondrial mechanism of heat stress-induced injury in rat cardiomyocyte. Cell Stress & Chaperones, 9, 281-293.
104. Rand, D.M. (2001) The units of selection on mitochondrial DNA. Annual Review of Ecology and Systematics, 32, 415-448.
105. Rando, O.J. & Verstrepen, K.J. (2007) Timescales of genetic and epigenetic inheritance. Cell, 128, 655-668.
106. Rawson, P.D. & Burton, R.S. (2002) Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proceedings of the National Academy of Science of the United States of America, 99, 12955-12958.
107. Rhee, S.G., Bae, Y.S., Lee, S.R. & Kwon, J. (2000) Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Science's STKE: Signal Transduction Knowledge Environment, 2000, pe1.
108. Robison, B.D., Wheeler, P.A. & Thorgaard, G.H. (1999) Variation in development rate among clonal lines of rainbow trout (Oncorhynchus mykiss). Aquaculture, 173, 131-141.
109. Rogina, B., Reenan, R.A., Nilsen, S.P. & Helfand, S.L. (2000) Extended life-span conferred by cotransporter gene mutations in Drosophila. Science, 290, 2137-2140.
110. Rose, G., Passarino, G., Carrieri, G., Altomare, K., Greco, V., Bertolini, S. et al. (2001) Paradoxes in longevity: sequence analysis of mtDNA haplogroup J in centenarians. European Journal of Human Genetics: EJHG, 9, 701-707.
111. Rose, G., Romeo, G., Dato, S., Crocco, P., Bruni, A.C., Hervonen, A. et al. (2010) Somatic point mutations in mtDNA control region are influenced by genetic background and associated with healthy aging: a GEHA study. PLoS One, 5, e13395.
112. Roubertoux, P.L., Sluyter, F., Carlier, M., Marcet, B., Maarouf-Veray, F., Cherif, C. et al. (2003) Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nature Genetics, 35, 65-69.
113. Ruiz-Pesini, E., Lott, M.T., Procaccio, V., Poole, J.C., Brandon, M.C., Mishmar, D. et al. (2007) An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Research, 35, D823-D828.
114. Safdar, A., Little, J.P., Stokl, A.J., Hettinga, B.P., Akhtar, M. & Tarnopolsky, M.A. (2011) Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. The Journal of Biological Chemistry, 286, 10605-10617.
115. Sagan, L. (1967) On the origin of mitosing cells. Journal of Theoretical Biology, 14, 255-274.
116. Sanz, A., Fernandez-Ayala, D.J., Stefanatos, R.K. & Jacobs, H.T. (2010) Mitochondrial ROS production correlates with, but does not directly regulate lifespan in Drosophila. Aging, 2, 200-223.
117. Schapira, A.H. (2008) Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurology, 7, 97-109.
118. Schieke, S.M., Phillips, D., McCoy, J.P. Jr, Aponte, A.M., Shen, R.F., Balaban, R.S. et al. (2006) The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. The Journal of Biological Chemistry, 281, 27643-27652.
119. Schizas, N.V., Chandler, G.T., Coull, B.C., Klosterhaus, S.L. & Quattro, J.M. (2001) Differential survival of three mitochondrial lineages of a marine benthic copepod exposed to a pesticide mixture. Environmental Science and Technology, 35, 535-538.
120. Sena, L.A. & Chandel, N.S. (2012) Physiological roles of mitochondrial reactive oxygen species. Molecular Cell, 48, 158-167.
121. Sharpley, M.S., Marciniak, C., Eckel-Mahan, K., McManus, M., Crimi, M., Waymire, K. et al. (2012) Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell, 151, 333-343.
122. Shimura, H., Hattori, N., Kubo, S., Mizuno, Y., Asakawa, S., Minoshima, S. et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nature Genetics, 25, 302-305.
123. Shoval, O., Sheftel, H., Shinar, G., Hart, Y., Ramote, O., Mayo, A. et al. (2012) Evolutionary trade-off's, Pareto optimality, and the geometry of phenotype space. Science, 336, 1157-1160.
124. Simpson, S.J. & Raubenheimer, D. (2012) The Nature of Nutrition. A Unifying Framework from Animal Adaptation to Human Obesity, 1 edn. Princeton University Press, Princeton and Oxford.
125. Smith, J.M. & Haigh, J. (1974) The hitch-hiking effect of a favourable gene. Genetical Research, 23, 23-35.
126. Somero, G.N. (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integrative and Comparative Biology, 42, 780-789.
127. Spitz, D.R., Azzam, E.I., Li, J.J. & Gius, D. (2004) Review: metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Reviews, 23, 311-322.
128. Stenesen, D., Suh, J.M., Seo, J., Yu, K., Lee, K.S., Kim, J.S. et al. (2013) Adenosine nucleotide biosynthesis and AMPK regulate adult life span and mediate the longevity benefit of caloric restriction in flies. Cell Metabolism, 17, 101-112.
129. Stewart, J.B., Freyer, C., Elson, J.L., Wredenberg, A., Cansu, Z., Trifunovic, A. et al. (2008) Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biology, 6, e10.
130. Stichel, C.C., Zhu, X.R., Bader, V., Linnartz, B., Schmidt, S. & Lubbert, H. (2007) Mono- and double-mutant mouse models of Parkinson's disease display severe mitochondrial damage. Human Molecular Genetics, 16, 2377-2393.
131. Suen, D.F., Narendra, D.P., Tanaka, A., Manfredi, G. & Youle, R.J. (2010) Parkin overexpression selects against a deleterious mtDNA mutation in heteroplasmic cybrid cells. Proceedings of the National Academy of Science of the United States of America, 107, 11835-11840.
132. Sun, C., Kong, Q.P. & Zhang, Y.P. (2007) The role of climate in human mitochondrial DNA evolution: a reappraisal. Genomics, 89, 338-342.
133. Sykes, B. (2001) The Seven Daughters of Eve. Bantam Press, London, New York.
134. Tanhauser, S.M. & Laipis, P.J. (1995) Multiple deletions are detectable in mitochondrial DNA of aging mice. The Journal of Biological Chemistry, 270, 24769-24775.
135. Teleman, A.A., Hietakangas, V., Sayadian, A.C. & Cohen, S.M. (2008) Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metabolism, 7, 21-32.
136. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J.N., Rovio, A.T., Bruder, C.E. et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 429, 417-423.
137. Tiefenböck, S.K., Baltzer, C., Egli, N.A. & Frei, C. (2010) The Drosophila PGC-1 homologue Spargel coordinates mitochondrial activity to insulin signalling. EMBO Journal, 29, 171-183.
138. Trounce, I.A., Kim, Y.L., Jun, A.S. & Wallace, D.C. (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods in Enzymology, 264, 484-509.
139. Tsutsui, H., Ide, T. & Kinugawa, S. (2006) Mitochondrial oxidative stress, DNA damage, and heart failure. Antioxidants & Redox Signaling, 8, 1737-1744.
140. Wai, T., Teoli, D. & Shoubridge, E.A. (2008) The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nature Genetics, 40, 1484-1488.
141. Walker, D.W., McColl, G., Jenkins, N.L., Harris, J. & Lithgow, G.J. (2000) Natural selection: Evolution of lifespan in C. elegans. Nature, 405, 296-297.
142. Wallace, D.C. (1999) Mitochondrial diseases in man and mouse. Science, 283, 1482-1488.
143. Wallace, D.C. (2013) Bioenergetics in human evolution and disease: implications for the origins of biological complexity and the missing genetic variation of common diseases. Philosophical Transactions of the Royal Society of London B Biological Science, 368, 20120267.
144. Wang, Y., Michikawa, Y., Mallidis, C., Bai, Y., Woodhouse, L., Yarasheski, K.E. et al. (2001) Muscle-specific mutations accumulate with aging in critical human mtDNA control sites for replication. Proceedings of the National Academy of Science of the United States of America, 98, 4022-4027.
145. Wang, P.Y., Neretti, N., Whitaker, R., Hosier, S., Chang, C., Lu, D. et al. (2009) Long-lived Indy and calorie restriction interact to extend life span. Proceedings of the National Academy of Science of the United States of America, 106, 9262-9267.
146. Wares, J.P., Barber, P.H., Ross-Ibarra, J., Sotka, E.E. & Toonen, R.J. (2006) Mitochondrial DNA and population size. Science, 314, 1388-1390; author reply 1388-1390.
147. Wenz, T., Rossi, S.G., Rotundo, R.L., Spiegelman, B.M. & Moraes, C.T. (2009) Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proceedings of the National Academy of Science of the United States of America, 106, 20405-20410.
148. White, D.J. & Gemmell, N.J. (2009) Can indirect tests detect a known recombination event in human mtDNA? Molecular Biology and Evolution, 26, 1435-1439.
149. Whitelaw, N.C. & Whitelaw, E. (2006) How lifetimes shape epigenotype within and across generations. Human Molecular Genetics, 15 (Spec No 2), R131-R137.
150. Willett, C.S. & Burton, R.S. (2003) Environmental influences on epistatic interactions: viabilities of cytochrome c genotypes in interpopulation crosses. Evolution, 57, 2286-2292.
151. Williams, G.C. (1957) Pleiotropy, natural-selection, and the evolution of senescence. Evolution, 11, 398-411.
152. Wolff, J.N., White, D.J., Woodhams, M., White, H.E. & Gemmel, N.J. (2011) The strength and timing of the mitochondrial bottleneck in salmon suggests a conserved mechanism in vertebrates. PLoS One, 6, e20522.
153. Wolff, J.N., Nafisinia, M., Sutovsky, P. & Ballard, J.W.O. (2013) Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans. Heredity (Edinb), 110, 57-62.
154. Xu, H., DeLuca, S.Z. & O'Farrell, P.H. (2008) Manipulating the metazoan mitochondrial genome with targeted restriction enzymes. Science, 321, 575-577.
155. Yee, W.K.W., Sutton, K.L. & Dowling, D.K. (2013) In vivo male fertility is affected by naturally occurring mitochondrial haplotypes. Current Biology, 23, R55-R56.
156. Yoneda, M., Chomyn, A., Martinuzzi, A., Hurko, O. & Attardi, G. (1992) Marked replicative advantage of human mtDNA carrying a point mutation that causes the MELAS encephalomyopathy. Proceedings of the National Academy of Science of the United States of America, 89, 11164-11168.
157. Yui, R., Ohno, Y. & Matsuura, E.T. (2003) Accumulation of deleted mitochondrial DNA in aging Drosophila melanogaster. Genes & Genetic Systems, 78, 245-251.
158. Zemach, A., McDaniel, I.E., Silva, P. & Zilberman, D. (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science, 328, 916-919.
159. Zukiene, R., Nauciene, Z., Ciapaite, J. & Mildaziene, V. (2010) Acute temperature resistance threshold in heart mitochondria: febrile temperature activates function but exceeding it collapses the membrane barrier. International Journal of Hyperthermia, 26, 56-66.