Revealing the hidden complexities of mtDNA inheritance

Molecular Ecology

Volumn 17, Issue 23, 2008, Pages 4925-4942

  White, Daniel James ^a   Wolff, Jonci Nikolai ^b   Pierson, Melanie ^c   Gemmell, Neil John ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF CANTERBURY   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Implications; Inheritance; mtDNA; Nonclonality

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; GENETIC RECOMBINATION; GENETIC SELECTION; GENETICS; HUMAN; MITOCHONDRIAL GENE; MOLECULAR EVOLUTION; MUTATION; REVIEW;

ANIMALS; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENES, MITOCHONDRIAL; HUMANS; MUTATION; RECOMBINATION, GENETIC; SELECTION (GENETICS);

EID: 56549131066     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2008.03982.x     Document Type: Review

References (201)

1. Abbott CL, Double MC, Trueman JWH, Robinson A, Cockburn A (2005) An unusual source of apparent mitochondrial heteroplasmy: duplicate mitochondrial control regions in Thalassarche albatrosses. Molecular Ecology, 14, 3605 3613.
2. Adkins RM (2004) Comparison of the accuracy of methods of computational haplotype inference using a large empirical dataset. BMC Genetics, 5 : 22.
3. Allen JF (1996) Separate sexes and the mitochondrial theory of ageing. Journal of Theoretical Biology, 180, 135 140.
4. Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proceedings of the National Academy of Sciences, USA, 93, 13859 13863.
5. Armstrong MR, Husmeier D, Phillips MS, Blok VC (2007) Segregation and recombination of a multipartite mitochondrial DNA in populations of the potato cyst nematode Globodera pallida. Journal of Molecular Evolution, 64, 689 701.
6. Arunkumar KP, Metta M, Nagaraju J (2006) Molecular phylogeny of silkmoths reveals the origin of domesticated silkmoth, Bombyx mori from Chinese Bombyx mandarina and paternal inheritance of Antheraea proylei mitochondrial DNA. Molecular Phylogenetics and Evolution, 40, 419 427.
7. Ashley MV, Laipis PJ, Hauswirth WW (1989) Rapid segregation of heteroplasmic bovine mitochondria. Nucleic Acids Research, 17, 7325 7331.
8. Avise JC, Lansman RA, Shade RO (1979) The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics, 92, 279 295.
9. Avise JC, Arnold J, Ball RM et al 1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics, 18, 489 522.
10. Awadalla P, Eyre-Walker A, Smith JM (1999) Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science, 286, 2524 2525.
11. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729 744.
12. Barr CM, Neiman M, Taylor DR (2005) Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist, 168, 39 50.
13. Bass AL, Good DA, Bjorndal KA et al 1996) Testing models of female reproductive migratory behaviour and population structure in the Caribbean hawksbill turtle, Eretmochelys imbricata, with mtDNA sequences. Molecular Ecology, 5, 321 328.
14. Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics, 152, 763 773.
15. Bendall KE, Macaulay VA, Baker JR, Sykes BC (1996) Heteroplasmic point mutations in the human mtDNA control region. American Journal of Human Genetics, 59, 1276 1287.
16. Bensasson D, Zhang DX, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology & Evolution, 16, 314 321.
17. Bergstrom CT, Pritchard J (1998) Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics, 149, 2135 2146.
18. Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature, 424, 197 201.
19. Beziat F, Touraille S, Debise R et al 1997) Biochemical and molecular consequences of massive mitochondrial gene loss in different tissues of a mutant strain of Drosophila subobscura. Journal of Biological Chemistry, 272, 22583 22590.
20. Birky CW (1978) Transmission genetics of mitochondria and chloroplasts. Annual Review of Genetics, 12, 471 512.
21. Birky CW Jr. (1994) Relaxed and stringent genomes: why cytoplasmic genes don't obey Mendel's laws. Journal of Heredity, 85, 355 365.
22. Birky CW Jr. (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proceedings of the National Academy of Sciences, USA, 92, 11331 11338.
23. Birky CW (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annual Review of Genetics, 35, 125 148.
24. Birky CW, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift-equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics, 121, 613 627.
25. Blok RB, Gook DA, Thorburn DR, Dahl HHM (1997) Skewed segregation of the mtDNA nt 8993 (T→G) mutation in human oocytes. American Journal of Human Genetics, 60, 1495 1501.
26. Bogenhagen DF (1999) Repair of mtDNA in vertebrates. American Journal of Human Genetics, 64, 1276 1281.
27. Bogenhagen DF, Rousseau D, Burke S (2008) The layered structure of human mitochondrial DNA nucleoids. Journal of Biological Chemistry, 283, 3665 3675.
28. Brandstatter A, Niederstatter H, Parson W (2004) Monitoring the inheritance of heteroplasmy by computer-assisted detection of mixed basecalls in the entire human mitochondrial DNA control region. International Journal of Legal Medicine, 118, 47 54.
29. Breton S, Beaupre HD, Stewart DT, Hoeh WR, Blier PU (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn't one enough? Trends in Genetics, 23, 465 474.
30. Bromham L, Eyre-Walker A, Smith NH, Maynard Smith J (2003) Mitochondrial Steve: paternal inheritance of mitochondria in humans. Trends in Ecology & Evolution, 18, 2 4.
31. Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences, USA, 76, 1967 1971.
32. Bruen TC, Philippe H, Bryant D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics, 172, 2665 2681.
33. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends in Genetics, 19, 709 716.
34. Burzynski A, Zbawicka M, Skibinski DOF, Wenne R (2006) Doubly uniparental inheritance is associated with high polymorphism for rearranged and recombinant control region haplotypes in Baltic Mytilus trossulus. Genetics, 174, 1081 1094.
35. Cann RL, Stoneking M, Wilson AC (1987) Mitochondrial DNA and human evolution. Nature (London), 325, 31 36.
36. Cao L, Shitara H, Horii T et al 2007) The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nature Genetics, 39, 386 390.
37. Chan DC (2006) Mitochondrial fusion and fission in mammals. Annual Review of Cell and Developmental Biology, 22, 79 99.
38. Charlesworth D, Morgan MT, Charlesworth B (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genetical Research, 61, 39 56.
39. Chinnery PF, Thorburn DR, Samuels DC et al 2000) The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends in Genetics, 16, 500 505.
40. Chomyn A, Martinuzzi A, Yoneda M et al 1992) Melas mutation in mtDNA binding-site for transcription termination factor causes defects in protein-synthesis and in respiration but no change in levels of upstream and downstream mature transcripts. Proceedings of the National Academy of Sciences, USA, 89, 4221 4225.
41. Ciborowski KL, Consuegra S, de Leaniz CG et al 2007) Rare and fleeting: an example of interspecific recombination in animal mitochondrial DNA. Biology Letters, 3, 554 557.
42. Clark AG (1990) Inference of haplotypes from PCR-amplified samples of diploid populations. Molecular Biology and Evolution, 7, 111 122.
43. Collura RV, Stewart CB (1995) Insertions and duplications of mtDNA in the nuclear genomes of old-world monkeys and hominoids. Nature, 378, 485 489.
44. Cree LM, Samuels DC, de Sousa Lopes SC et al 2008) A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nature Genetics, 40, 249 254.
45. Dawid IB, Blackler AW (1972) Maternal and cytoplasmic inheritance of mitochondrial DNA in Xenopus. Developmental Biology, 29, 152 161.
46. Eberhard JR, Wright TF, Bermingham E (2001) Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Molecular Biology and Evolution, 18, 1330 1342.
47. Ekstrand MI, Falkenberg M, Rantanen A et al 2004) Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Human Molecular Genetics, 13, 935 944.
48. Elson JL, Lightowlers RN (2006) Mitochondrial DNA clonality in the dock: can surveillance swing the case? Trends in Genetics, 22, 603 607.
49. Ephrussi B, Demargeriehottinguer H, Roman H (1955) Suppressiveness - a new factor in the genetic determinism of the synthesis of respiratory enzymes in yeast. Proceedings of the National Academy of Sciences, USA, 41, 1065 1071.
50. Ernster L, Schatz G (1981) Mitochondria - a historical review. Journal of Cell Biology, 91, S227 S255.
51. Eyre-Walker A (2000) Do mitochondria recombine in humans? Philosophical Transactions of the Royal Society B: Biological Sciences, 355, 1573 1580.
52. Eyre-Walker A, Smith NH, Smith JM (1999) How clonal are human mitochondria? Proceedings of the Royal Society B: Biological Sciences, 266, 477 483.
53. Fan W, Waymire KG, Narula N et al 2008) A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science, 319, 958 962.
54. Felsenstein J (1989) phylip - Phylogeny Inference Package (Version 3.2). Cladistics, 5, 164 166.
55. Fleming TP, Javed Q, Hay M (1992) Epithelial differentiation and intercellular junction formation in the mouse early embryo. Development Supplement, 17, 105 112.
56. Fontaine KM, Cooley JR, Simon C (2007) Evidence for paternal leakage in hybrid periodical cicadas (Hemiptera: Magicicada spp.). PLoS ONE, 2, e892.
57. Francisco JF, Brown GG, Simpson MV (1979) Further studies on types A and B rat mtDNAs: cleavage maps and evidence for cytoplasmic inheritance in mammals. Plasmid, 2, 426 436.
58. Gantenbein B, Fet V, Gantenbein-Ritter IA, Balloux F (2005) Evidence for recombination in scorpion mitochondrial DNA (Scorpiones: Buthidae). Proceedings of the Royal Society B: Biological Sciences, 272, 697 704.
59. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proceedings of the Royal Society B: Biological Sciences, 77, 6715 6719.
60. Gill P, Ivanov PL, Kimpton C et al 1994) Identification of the remains of the Romanov family by DNA analysis. Nature Genetics, 6, 130 135.
61. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science, 283, 1476 1481.
62. Guo X, Liu S, Liu Y (2006) Evidence for recombination of mitochondrial DNA in triploid crucian carp. Genetics, 172, 1745 1749.
63. Gyllensten U, Wharton D, Wilson AC (1985) Maternal inheritance of mitochondrial DNA during backcrossing of two species of mice. Journal of Heredity, 76, 321 324.
64. Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial-DNA in mice. Nature, 352, 255 257.
65. Hagelberg E, Goldman N, Lio P et al 2000) Evidence for mitochondrial DNA recombination in a human population of island Melanesia: correction. Proceedings of the Royal Society B: Biological Sciences, 267, 1595 1596.
66. Hastings IM (1992) Population genetic aspects of deleterious cytoplasmic genomes and their effect on the evolution of sexual reproduction. Genetical Research, 59, 215 225.
67. Hauswirth WW, Laipis PJ (1982) Mitochondrial DNA polymorphism in a maternal lineage of Holstein cows. Proceedings of the National Academy of Sciences, USA, 79, 4686 4690.
68. Hayashi JI, Yonekawa H, Gotoh O, Watanabe J, Tagashira Y (1978) Strictly maternal inheritance of rat mitochondrial DNA. Biochemical and Biophysical Research Communications, 83, 1032 1038.
69. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270, 313 321.
70. Hecht NB, Liem H, Kleene KC, Distel RJ, Ho SM (1984) Maternal inheritance of the mouse mitochondrial genome is not mediated by a loss or gross alteration of the paternal mitochondrial DNA or by methylation of the oocyte mitochondrial DNA. Developmental Biology, 102, 452 461.
71. Hirano M, Shtilbans A, Mayeux R et al 1997) Apparent mtDNA heteroplasmy in Alzheimer's disease patients and in normals due to PCR amplification of nucleus-embedded mtDNA pseudogenes. Proceedings of the National Academy of Sciences, USA, 94, 14894 14899.
72. Hiraoka J-I, Hirao Y-H (1988) Fate of sperm tail components after incorporation into the hamster egg. Gamete Research, 19, 369 380.
73. Hoarau G, Holla S, Lescasse R, Stam WT, Olsen JL (2002) Heteroplasmy and evidence for recombination in the mitochondrial control region of the flatfish Platichthys flesus. Molecular Biology and Evolution, 19, 2261 2264.
74. Hogan B, Constantini F, Lacey E (1986) Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
75. Holt IJ, Dunbar DR, Jacobs HT (1997) Behaviour of a population of partially duplicated mitochondrial DNA molecules in cell culture: Segregation, maintenance and recombination dependent upon nuclear background. Human Molecular Genetics, 6, 1251 1260.
76. Holt IJ, Harding AE, Petty RKH, Morganhughes JA (1990) A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. American Journal of Human Genetics, 46, 428 433.
77. Howell N, Halvorson S, Kubacka I et al 1992) Mitochondrial gene segregation in mammals: is the bottleneck always narrow? Human Genetics, 90, 117 120.
78. Hurst LD (1996) Why are there only two sexes? Proceedings of the Royal Society B: Biological Sciences, 263, 415 422.
79. Hurst LD, Hamilton WD (1992) Cytoplasmic fusion and the nature of sexes. Proceedings of the Royal Society B: Biological Sciences, 247, 189 194.
80. Hurst LD, Peck JR (1996) Recent advances in understanding of the evolution and maintenance of sex. Trends in Ecology & Evolution, 11, A46 A52.
81. Hutchison CA, 3rd. Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature, 251, 536 538.
82. Ingman M, Kaessmann H, Paabo S, Gyllensten U (2000) Mitochondrial genome variation and the origin of modern humans. Nature, 408, 708 713.
83. Innan H, Nordborg M (2002) Recombination or mutational hot spots in human mtDNA? Molecular Biology and Evolution, 19, 1122 1127.
84. Ivanov PL, Wadhams MJ, Roby RK et al 1996) Mitochondrial DNA sequence heteroplasmy in the Grand Duke of Russia Georgij Romanov establishes the authenticity of the remains of Tsar Nicholas II. Nature Genetics, 12, 417 420.
85. Jansen RP, de Boer K (1998) The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Molecular and Cellular Endocrinology, 145, 81 88.
86. Jenuth JP, Peterson AC, Fu K, Shoubridge EA (1996) Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nature Genetics, 14, 146 151.
87. Jorde LB, Bamshad M (2000) Questioning evidence for recombination in human mitochondrial DNA. Science, 288, 1931a.
88. Kaneda H, Hayashi J, Takahama S et al 1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proceedings of the National Academy of Sciences, USA, 92, 4542 4546.
89. Kann LM, Rosenblum EB, Rand DM (1998) Aging, mating, and the evolution of mtDNA heteroplasmy in Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA, 95, 2372 2377.
90. Kaplan NL, Hudson RR, Langley CH (1989) The hitchhiking effect revisited. Genetics, 123, 887 899.
91. Khrapko K (2008) Two ways to make an mtDNA bottleneck. Nature Genetics, 40, 134 135.
92. Kimura M, Ohta T (1969) Average number of generations until fixation of a mutant gene in a finite population. Genetics, 61, 763 771.
93. Kimura M, Ohta T (1971) Theoretical Aspects of Population Genetics. Princeton University Press, Princeton, New Jersey.
94. Kirch PV (2000) On the Road of the Winds: An Archaeological History of the Pacific Islands before European Contact. University of California Press, Berkeley, California.
95. Kivisild T, Shen PD, Wall DP et al 2006) The role of selection in the evolution of human mitochondrial genomes. Genetics, 172, 373 387.
96. Kivisild T, Villems R (2000) Questioning evidence for recombination in human mitochondrial DNA. Science, 288, 1931a.
97. Kmiec B, Woloszynska M, Janska H (2006) Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Current Genetics, 50, 149 159.
98. Kocher TD, Thomas WK, Meyer A et al 1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA, 86, 6196 6200.
99. Koehler CM, Lindberg GL, Brown DR et al 1991) Replacement of bovine mitochondrial DNA by a sequence variant within one generation. Genetics, 129, 247 255.
100. Kondo R, Satta Y, Matsuura ET et al 1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics, 126, 657 663.
101. Kraytsberg Y, Schwartz M, Brown TA et al 2004) Recombination of human mitochondrial DNA. Science, 304, 981 981.
102. Kroon AM, de Vos WM, Bakker H (1978) The heterogeneity of rat-liver mitochondrial DNA. Biochimica et Biophysica Acta, 519, 269 273.
103. Kucej M, Butow RA (2007) Evolutionary tinkering with mitochondrial nucleoids. Trends in Cell Biology, 17, 586 592.
104. Kuhner MK, Yamato J, Felsenstein J (1995) Estimating effective population-size and mutation-rate from sequence data using Metropolis-Hastings sampling. Genetics, 140, 1421 1430.
105. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics, 149, 429 434.
106. Kumazawa Y, Ota H, Nishida M, Ozawa T (1996) Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Molecular Biology and Evolution, 13, 1242 1254.
107. Kvist L, Martens J, Nazarenko A, Orell M (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Molecular Biology and Evolution, 20, 243 247.
108. Ladoukakis ED, Zouros E (2001a) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Molecular Biology and Evolution, 18, 1168 1175.
109. Ladoukakis ED, Zouros E (2001b) Recombination in animal mitochondrial DNA: evidence from published sequences. Molecular Biology and Evolution, 18, 2127 2131.
110. Lakshmipathy U, Campbell C (1999a) Double strand break rejoining by mammalian mitochondrial extracts. Nucleic Acids Research, 27, 1198 1204.
111. Lakshmipathy U, Campbell C (1999b) The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Molecular and Cellular Biology, 19, 3869 3876.
112. Larsson NG, Wang J, Wilhelmsson H et al 1998) Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nature Genetics, 18, 231 236.
113. Lee JS, Miya M, Lee YS et al 2001) The complete DNA sequence of the mitochondrial genome of the self-fertilizing fish Rivulus marmoratus (Cyprinodontiformes, Rivulidae) and the first description of duplication of a control region in fish. Gene, 280, 1 7.
114. Legros F, Malka F, Frachon P, Lombes A, Rojo M (2004) Organ-ization and dynamics of human mitochondrial DNA. Journal of Cell Science, 117, 2653 2662.
115. Liau WS, Gonzalez-Serricchio AS, Deshommes C, Chin K, LaMunyon CW (2007) A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genetics, 8.
116. Loeb LA (2001) A mutator phenotype in cancer. Cancer Research, 61, 3230 3239.
117. Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature, 387, 247 247.
118. MacAlpine DM, Perlman PS, Butow RA (1998) The high mobility group protein Abf2p influences the level of yeast mitochondrial DNA recombination intermediates in vivo. Proceedings of the National Academy of Sciences, USA, 95, 6739 6743.
119. Macaulay V, Richards M, Sykes B (1999) Mitochondrial DNA recombination - no need to panic. Proceedings of the Royal Society of London, Series B: Biological Sciences, 266, 2037 2039.
120. Magoulas A, Zouros E (1993) Restriction-site heteroplasmy in anchovy (Engraulis encrasicolus) indicates incidental biparental inheritance of mitochondrial DNA. Molecular Biology and Evolution, 10, 319 325.
121. Malka F, Lombes A, Rojo M (2006) Organization, dynamics and transmission of mitochondrial DNA: focus on vertebrate nucleoids. Biochimica et Biophysica Acta, 1763, 463 472.
122. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiology, 118, 9 17.
123. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics, 21, 260 262.
124. Mate ML, Di Rocco F, Zambelli A, Vidal-Rioja L (2007) Mitochondrial heteroplasmy in control region DNA of South American camelids. Small Ruminant Research, 71, 123 129.
125. Meusel MS, Moritz RFA (1993) Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis mellifera L.) eggs. Current Genetics, 24, 539 543.
126. Millar CD, Dodd A, Anderson J et al 2008) Mutation and Evolutionary Rates in Adélie Penguins from the Antarctic. Public Library of Science, Genetics, 4, el000204.
127. Milligan BG (1992) Is Organelle DNA Strictly maternally inherited - power analysis of a binomial-distribution. American Journal of Botany, 79, 1325 1328.
128. Mishmar D, Ruiz-Pesini E, Golik P et al 2003) Natural selection shaped regional mtDNA variation in humans. Proceedings of the National Academy of Sciences, USA, 100, 171 176.
129. Mjelle KA, Karlsen BO, Jorgensen TE, Moum T, Johansen SD (2008) Halibut mitochondrial genomes contain extensive hetero-plasmic tandem repeat arrays involved in DNA recombination. BMC Genomics, 9, 10.
130. Moritz C, Dowling TE, Brown WM (1987) Evolution of animal mitochondrial DNA: Relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18, 269 292.
131. Mounolou JC, Lacroute F (2005) Mitochondrial DNA: an advance in eukaryotic cell biology in the 1960s. Biology of the Cell, 97, 743 748.
132. Niu TH (2004) Algorithms for inferring haplotypes. Genetic Epidemiology, 27, 334 347.
133. Parr RL, Maki J, Reguly B et al 2006) The pseudo-mitochondrial genome influences mistakes in heteroplasmy interpretation. BMC Genomics, 7, 185.
134. Petit N, Touraille S, Debise R et al 1998) Developmental changes in heteroplasmy level and mitochondrial gene expression in a Drosophila subobscura mitochondrial deletion mutant. Current Genetics, 33, 330 339.
135. Pierson MJ (2007) Deciphering the mtDNA record of prehistoric population movements in Oceania. Biological Sciences. University of Canterbury, Christchurch, New Zealand.
136. Pierson MJ, Martinez-Arias R, Holland BR et al 2006) Deciphering past human population movements in Oceania: Provably optimal trees of 127 mtDNA genomes. Molecular Biology and Evolution, 23, 1966 1975.
137. Piganeau G, Gardner M, Eyre-Walker A (2004) A broad survey of recombination in animal mitochondria. Molecular Biology and Evolution, 21, 2319 2325.
138. Piko L, Taylor KD (1987) Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Developmental Biology, 123, 364 374.
139. Pontkingdon GA, Okada NA, Macfarlane JL et al 1995) A coral mitochondrial mutS gene. Nature, 375, 109 111.
140. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proceedings of the National Academy of Sciences, USA, 98, 13757 13762.
141. Posada D, Crandall KA (2002) The effect of recombination on the accuracy of phylogeny estimation. Journal of Molecular Evolution, 54, 396 402.
142. Posada D, Crandall KA, Holmes EC (2002) Recombination in evolutionary genomics. Annual Review of Genetics, 36, 75 97.
143. Rand DM (2001) The units of selection on mitochondrial DNA. Annual Review of Ecology and Systematics, 32, 415 448.
144. Rand DM, Harrison RG (1986) Mitochondrial DNA transmission genetics in crickets. Genetics, 114, 955 970.
145. Rannala B, Bertorelle G (2001) Using linked markers to infer the age of a mutation. Human Mutation, 18, 87 100.
146. Reilly JG, Thomas CA Jr. (1980) Length polymorphisms, restriction site variation, and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid, 3, 109 115.
147. Rispe C, Moran NA (2000) Accumulation of deleterious mutations in endosymbionts: Muller's ratchet with two levels of selection. American Naturalist, 156, 425 441.
148. Robertson BC, Steeves TE, McBride KP et al 2007) Phylogeography of the New Zealand blue duck (Hymenolaimus malacorhynchos): implications for translocation and species recovery. Conservation Genetics, 8, 1431 1440.
149. Rokas A, Ladoukakis E, Zouros E (2003) Animal mitochondrial DNA recombination revisited. Trends in Ecology & Evolution, 18, 411 417.
150. Ryan MT, Hoogenraad NJ (2007) Mitochondrial-nuclear communications. Annual Review of Biochemistry, 76, 701 722.
151. Santel A, Fuller MT (2001) Control of mitochondrial morphology by a human mitofusin. Journal of Cell Science, 114, 867 874.
152. Saraste M (1999) Oxidative phosphorylation at the fin de siecle. Science, 283, 1488 1493.
153. Satoh M, Kuroiwa T (1991) Organization of multiple nucleoids and DNA molecules in mitochondria of a human cell. Experimental Cell Research, 196, 137 140.
154. Schierup MH, Hein J (2000) Consequences of recombination on traditional phylogenetic analysis. Genetics, 156, 879 891.
155. Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends in Plant Science, 3, 175 180.
156. Schwartz M, Vissing J (2002) Paternal inheritance of mtDNA in a patient with mitochondrial myopathy. European Journal of Human Genetics, 10, 239 239.
157. Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annual Review of Biochemistry, 66, 409 435.
158. Sherengul W, Kondo R, Matsuura ET (2006) Analysis of paternal transmission of mitochondrial DNA in Drosophila. Genes and Genetic Systems, 81, 399 404.
159. Shitara H, Hayashi JI, Takahama S, Kaneda H, Yonekawa H (1998) Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage. Genetics, 148, 851 857.
160. Shoubridge EA, Wai T (2007) Mitochondrial DNA and the mammalian oocyte. Mitochondrion in the Germline and Early Development.
161. Slate J, Gemmell NJ (2004) Eve 'n' Steve: recombination of human mitochondrial DNA. Trends in Ecology & Evolution, 19, 561 563.
162. Smith LC, Bordignon V, Couto MM et al 2002) Mitochondrial genotype segregation and the bottleneck. Reproductive Biomedicine Online, 4, 248 255.
163. Solignac M, Génermont J, Monnerot M, Mounolou J-C (1984) Genetics of mitochondria in Drosophila: mtDNA inheritance in heteroplasmic strains of D. mauritiana. Molecular and General Genetics MGG, 197, 183 188.
164. Sorenson MD, Quinn TW (1998) NUMTs: a challenge for avian systematics and population biology. Auk, 115, 214 221.
165. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics, 68, 978 989.
166. Stewart JB, Freyer C, Elson JL et al 2008) Strong purifying selection in transmission of mammalian mitochondrial DNA. Public Library of Science, Biology, 6, e10.
167. Stoneking M (2000) Hypervariable sites in the mtDNA control region are mutational hotspots. American Journal of Human Genetics, 67, 1029 1032.
168. Sutovsky P, Moreno RD, Ramalho-Santos J et al 1999) Development - ubiquitin tag for sperm mitochondria. Nature, 402, 371 372.
169. Sutovsky P, Moreno RD, Ramalho-Santos J et al 2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biology of Reproduction, 63, 582 590.
170. Sutovsky P, McCauley TC, Sutovsky M, Day BN (2003) Early degradation of paternal mitochondria in domestic pig (Sus scrofa) is prevented by selective proteasomal inhibitors lactacystin and MG132. Biology of Reproduction, 68, 1793 1800.
171. Swofford DL (1996) paup: Phylogenetic Analysis Using Parsimony (and Other Methods), 4.0 ed. Sinauer Associates, Sunderland, Massachusetts.
172. Tamura K, Dudley J, Nei M, Kumar S (2007) mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Molecular Biology and Evolution, 24, 1596 1599.
173. Tang YY, Manfredi G, Hirano M, Schon EA (2000) Maintenance of human rearranged mitochondrial DNAs in long-term cultured transmitochondrial cell lines. Molecular Biology of the Cell, 11, 2349 2358.
174. Templeton AR (2002) Out of Africa again and again. Nature, 416, 45 51.
175. Theologidis L, Saavedra C, Zouros E (2007) No evidence for absence of paternal mtDNA in male progeny from pair matings of the mussel Mytilus galloprovincialis. Genetics, 176, 1367 1369.
176. Thompson WE, Ramalho-Santos J, Sutovsky P (2003) Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biology of Reproduction, 69, 254 260.
177. Thyagarajan B, Padua RA, Campbell C (1996) Mammalian mitochondria possess homologous DNA recombination activity. Journal of Biological Chemistry, 271, 27536 27543.
178. Tourmen Y, Baris O, Dessen P et al 2002) Structure and chromosomal distribution of human mitochondrial pseudogenes. Genomics, 80, 71 77.
179. Tsang WY, Lemire BD (2002) Mitochondrial genome content is regulated during nematode development. Biochemical and Biophysical Research Communications, 291, 8 16.
180. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E (2005) Widespread recombination in published animal mtDNA sequences. Molecular Biology and Evolution, 22, 925 933.
181. Ujvari B, Dowton M, Madsen T (2007) Mitochondrial DNA recombination in a free-ranging Australian lizard. Biology Letters, 3, 189 192.
182. Ursprung H, Schabtach E (1965) Fertilization in tunicates: loss of the paternal mitochondrion prior to sperm entry. Journal of Experimental Biology, 159, 379 383.
183. Vali U (2002) Mitochondrial pseudo-control region in Old World eagles (genus Aquila). Molecular Ecology, 11, 2189 2194.
184. Venetis C, Theologidis I, Zouros E, Rodakis GC (2006) No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proceedings of the Royal Society B: Biological Sciences, 273, 2483 2489.
185. Wallace DC (1999) Mitochondrial diseases in man and mouse. Science, 283, 1482 1488.
186. Westermann B (2002) Merging mitochondria matters: cellular role and molecular machinery of mitochondrial fusion. EMBO Reports, 3, 527 531.
187. White HE, Durston VJ, Seller A et al 2005) Accurate detection and quantitation of heteroplasmic mitochondrial point mutations by pyrosequencing. Genetic Testing, 9, 190 199.
188. White SL, Shanske S, McGill JJ et al 1999) Mitochondrial DNA mutations at nucleotide 8993 show a lack of tissue- or age-related variation. Journal of Inherited Metabolic Disease, 22, 899 914.
189. Williamson D (2002) Timeline - the curious history of yeast mitochondrial DNA. Nature Reviews Genetics, 3, 475 481.
190. Wiuf C, Christensen T, Hein J (2001) A simulation study of the reliability of recombination detection methods. Molecular Biology and Evolution, 18, 1929 1939.
191. Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Research, 12, 885 893.
192. Wolff JN, Gemmell NJ (2008a) Combining allele-specific fluorescent probes and restriction assay in real-time PCR to achieve SNP scoring beyond allele ratios of 1:1000. BioTechniques, 44, 193 199.
193. Wolff JN, Gemmell NJ (2008b) Lost in the zygote: the dilution of paternal mtDNA upon fertilization. Heredity, 101, 429 434.
194. Wolstenholme DR, Clary DO (1985) Sequence evolution of Drosophila mitochondrial DNA. Genetics, 109, 725 744.
195. Yaffe MP (1999) The machinery of mitochondrial inheritance and behavior. Science, 283, 1493 1497.
196. Yoneda M, Chomyn A, Martinuzzi A, Hurko O, Attardi G (1992) Marked replicative advantage of human mtDNA carrying a point mutation that causes the
197. Zhang DX, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology & Evolution, 11, 247 251.
198. Zhao X, Li N, Guo W et al 2004) Further evidence for paternal inheritance of mitochondrial DNA in the sheep (Ovis aries). Heredity, 93, 399 403.
199. Zouros E, Freeman KR, Ball AO, Pogson GH (1992) Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature, 359, 412 414.
200. Zsurka G, Kraytsberg Y, Kudina T et al 2005) Recombination of mitochondrial DNA in skeletal muscle of individuals with multiple mitochondrial DNA heteroplasmy. Nature Genetics, 37, 873 877.
201. Zsurka G, Hampel KG, Kudina T et al 2007) Inheritance of mitochondrial DNA recombinants in double-heteroplasmic families: potential implications for phylogenetic analysis. American Journal of Human Genetics, 80, 298 305.