Energy, ageing, fidelity and sex: Oocyte mitochondrial DNA as a protected genetic template

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1622, 2013, Pages

  de Paula, Wilson B M ^a   Lucas, Cathy H ^b   Agip, Ahmed Noor A ^a   Vizcay Barrena, Gema ^c   Allen, John F ^a,d  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b NATIONAL OCEANOGRAPHY CENTRE   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Aging; Aurelia aurita; Cytoplasmic inheritance; Maternal inheritance; Mitochondrial genome; Oxidative phosphorylation; Weismann barrier

Indexed keywords

DNA; EVOLUTIONARY BIOLOGY; FEMALE; FERTILIZATION (REPRODUCTION); FREE RADICAL; GAMETE; GENETIC ANALYSIS; JELLYFISH; MUTATION; SPECIES DIVERSITY;

ANIMALIA; AURELIA AURITA; EUKARYOTA; SCYPHOZOA;

MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

AGING; ANIMAL; CYTOLOGY; ENERGY METABOLISM; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION; GENETICS; JELLYFISH; MALE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; OOCYTE; PHYSIOLOGY; ULTRASTRUCTURE;

AGING; ANIMALS; DNA, MITOCHONDRIAL; ENERGY METABOLISM; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; OOCYTES; REACTIVE OXYGEN SPECIES; SCYPHOZOA;

EID: 84878784073     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0263     Document Type: Article

References (106)

1. Mitchell P. 1961 Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191, 144-148. (doi:10. 1038/191144a0)
2. Roodyn DB, Wilkie D. 1968 The biogenesis of mitochondria. London: Methuen.
3. Haslbrunner E, Tuppy H, Schatz G. 1964 Deoxyribonucleic acid associated with yeast mitochondria. Biochem. Biophys. Res. Commun. 15, 127-132. (doi:10.1016/0006- 291X(64)90311-0)
4. Horner DS, Hirt RP, Kilvington S, Lloyd D, Embley TM. 1996 Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. Lond. B 263, 1053-1059. (doi:10.1098/rspb.1996.0155)
5. Martin W, Müller M. 2007 Origin of mitochondria and hydrogenosomes. Berlin, Heidelberg: Springer.
6. Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR. 1985 Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443-4447. (doi:10.1073/pnas.82.13.4443)
7. Sagan L. 1967 On the origin of mitosing cells. J. Theor. Biol. 14, 255-274. (doi:10.1016/0022- 5193(67)90079-3)
8. Nass MM, Nass S. 1963 Intramitochondrial fibers with DNA characteristics. I. Fixation and electron staining reactions. J. Cell Biol. 19, 593-611. (doi:10.1083/jcb.19.3.593)
9. Luck DJL, Reich E. 1964 DNA in mitochondria of Neurospora crassa. Proc. Natl Acad. Sci. USA 52, 931-938. (doi:10.1073/pnas.52.4.931)
10. Anderson S et al. 1981 Sequence and organization of the human mitochondrial genome. Nature 290, 457-465. (doi:10.1038/290457a0)
11. Pesole G, Allen JF, Lane N, Martin W, Rand DM, Schatz G, Saccone C. 2012 The neglected genome. EMBO Rep. 13, 473-474. (doi:10.1038/ embor.2012.57)
12. Claros MG, Perea J, Shu Y, Samatey FA, Popot JL, Jacq C. 1995 Limitations to in vivo import of hydrophobic proteins into yeast mitochondria: the case of a cytoplasmically synthesized apocytochrome b. Eur. J. Biochem. 228, 762-771. (doi:10.1111/j.1432-1033.1995.0762m.x)
13. Koehler CM, Merchant S, Schatz G. 1999 How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem. Sci. 24, 428-432. (doi:10.1016/S0968-0004(99)01462-0)
14. Allen JF. 2003 The function of genomes in bioenergetic organelles. Phil. Trans. R. Soc. Lond. B 358, 19-38. (doi:10.1098/rstb.2002.1191)
15. Camus M, Clancy DJ, Dowling DK. 2012 Mitochondria, maternal inheritance, and male aging. Curr. Biol. 22, 1-5. (doi:10.1016/j.cub. 2011.12.009)
16. Wallace DC. 2007 Why do we still have a maternally inherited mitochondrial DNA? Insights from evolutionary medicine. Annu. Rev. Biochem. 76, 781-821. (doi:10.1146/annurev.biochem.76.081205.150955)
17. Whitehouse HLK. 1969 Towards an understanding of the mechanism of heredity, 2nd edn. London: Edward Arnold (Publishers) Ltd.
18. Allen JF, de Paula WB, Puthiyaveetil S, Nield J. 2011 A structural phylogenetic map for chloroplast photosynthesis. Trends Plant. Sci. 16, 645-655. (doi:10.1016/j.tplants.2011.10.004)
19. Allen JF. 1993 Control of gene-expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165, 609-631. (doi:10.1006/jtbi.1993.1210)
20. León-Avila G, Tovar J. 2004 Mitosomes of Entamoeba histolytica are abundant mitochondrionrelated remnant organelles that lack a detectable organellar genome. Microbiology 150, 1245-1250. (doi:10.1099/mic.0.26923-0)
21. Tovar J, Fischer A, Clark CG. 1999 The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013-1021. (doi:10.1046/j. 1365-2958.1999.01414.x)
22. Van Der Giezen M. 2009 Hydrogenosomes and mitosomes: conservation and evolution of functions. J. Eukaryot. Microbiol. 56, 221-231. (doi:10.1111/j. 1550-7408.2009.00407.x)
23. Williams BAP, Hirt RP, Lucocq JM, Embley TM. 2002 A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865-869. (doi:10.1038/nature00949)
24. Allen JF. 2003 Why chloroplasts and mitochondria contain genomes. Comp. Funct. Genomics 4, 31-36. (doi:10.1002/cfg.245)
25. Daley DO, Clifton R, Whelan J. 2002 Intracellular gene transfer: reduced hydrophobicity facilitates gene transfer for subunit 2 of cytochrome c oxidase. Proc. Natl Acad. Sci. USA 99, 10510-10515. (doi:10.1073/pnas.122354399)
26. Martin W, Hoffmeister M, Rotte C, Henze K. 2001 An overview of endosymbiotic models for the origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their heterotrophic lifestyle. Biol. Chem. 382, 1521-1539. (10.1515/BC.2001.187)
27. von Heijne G. 1986 Why mitochondria need a genome. FEBS Lett. 198, 1-4. (doi:10.1016/ 0014-5793(86)81172-3)
28. Race HL, Herrmann RG, Martin W. 1999 Why have organelles retained genomes? Trends Genet. 15, 364-370. (doi:10.1016/S0168-9525(99)01766-7)
29. Barbrook AC, Howe CJ, Purton S. 2006 Why are plastid genomes retained in non-photosynthetic organisms? Trends Plant Sci. 11, 101-108. (doi:10.1016/j.tplants.2005.12.004)
30. Pfannschmidt T, Nilsson A, Allen JF. 1999 Photosynthetic control of chloroplast gene expression. Nature 397, 625-628. (doi:10.1038/17624)
31. Puthiyaveetil S, Ibrahim IM, Jelicic B, Tomasic A, Fulgosi H, Allen JF. 2010 Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biol. Evol. 2, 888-896. (doi:10.1093/ evq073)
32. Allen CA, Håkansson G, Allen JF. 1995 Redox conditions specify the proteins synthesized by isolated- chloroplasts and mitochondria. Redox Rep. 1, 119-123.
33. de Paula WBM, Allen JF, van der Giezen M. 2012 Mitochondria, hydrogenosomes and mitosomes in relation to the CoRR hypothesis for genome function and evolution. In Organelle genetics (ed. CE Bullerwell), pp. 105-119. Berlin, Heidelberg: Springer.
34. Puthiyaveetil S et al. 2008 The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc. Natl Acad. Sci. USA 105, 10061-10066. (doi:10.1073/pnas.0803928105)
35. Puthiyaveetil S, Ibrahim IM, Allen JF. 2013 Evolutionary rewiring: a modified prokaryotic gene regulatory pathway in chloroplasts. Phil. Trans. R. Soc. B 367, 20120260. (doi:10.1098/ rstb20120260).
36. Allen JF, Raven JA. 1996 Free-radical-induced mutation vs redox regulation: costs and benefits of genes in organelles. J. Mol. Evol. 42, 482-492. (doi:10.1007/BF02352278)
37. Chance B, Sies H, Boveris A. 1979 Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527-605.
38. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. 2003 Production of reactive oxygen species by mitochondria: central role of complex III. J. Biol. Chem. 278, 36027-36031. (doi:10.1074/ jbc.M304854200)
39. Ohnishi ST, Shinzawa-Itoh K, Ohta K, Yoshikawa S, Ohnishi T. 2010 New insights into the superoxide generation sites in bovine heart NADH-ubiquinone oxidoreductase (complex I) The significance of protein-associated ubiquinone and the dynamic shifting of generation sites between semiflavin and semiquinone radicals. Bba-Bioenergetics 1797, 1901-1909. (doi:10.1016/j.bbabio.2010.05.012)
40. Kussmaul L, Hirst J. 2006 The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl Acad. Sci. USA 103, 7607-7612. (doi:10.1073/pnas.0510977103)
41. McCord JM, Fridovich I. 1969 Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244, 6049-6055.
42. Li Y et al. 1995 Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat. Genet. 11, 376-381. (doi:10.1038/ng1295-376)
43. Melov S, Schneider JA, Day BJ, Hinerfeld D, Coskun P, Mirra SS, Crapo JD, Wallace DC. 1998 A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18, 159-163. (doi:10.1038/ ng0298-159)
44. Taufer M, Peres A, de Andrade VM, de Oliveira G, Sa G, do Canto ME, dos Santos AR, Bauer ME, da Cruz IB. 2005 Is the Val16Ala manganese superoxide dismutase polymorphism associated with the aging process? J. Gerontol. A Biol. Sci. Med. Sci. 60, 432-438. (doi:10.1093/gerona/60.4.432)
45. Treiber N et al. 2011 Accelerated aging phenotype in mice with conditional deficiency for mitochondrial superoxide dismutase in the connective tissue. Aging Cell 10, 239-254. (doi:10.1111/j.1474-9726.2010.00658.x)
46. Pessayre D, Berson A, Fromenty B, Mansouri A. 2001 Mitochondria in steatohepatitis. Semin. Liver Dis. 21, 57-69. (doi:10.1055/s-2001-12929)
47. Berlett BS, Stadtman ER. 1997 Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272, 20313-20316. (doi:10.1074/jbc. 272.1.20)
48. Cooke MS, Evans MD, Dizdaroglu M, Lunec J. 2003 Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 17, 1195-1214. (doi:10.1096/fj. 02-0752rev)
49. Ames BN, Shigenaga MK, Hagen TM. 1993 Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl Acad. Sci. USA 90, 7915-7922. (doi:10.1073/pnas.90.17.7915)
50. Ames BN, Shigenaga MK, Hagen TM. 1995 Mitochondrial decay in aging. Biochim. Biophys. Acta 1271, 165-170. (doi:10.1016/0925- 4439(95)00024-X)
51. Harman D. 1972 The biologic clock: the mitochondria? J. Am. Geriatr. Soc. 20, 145-147.
52. Harman D. 1992 Free radical theory of aging. Mutat. Res. 275, 257-266. (doi:10.1016/0921-8734(92) 90030-S)
53. Shigenaga MK, Hagen TM, Ames BN. 1994 Oxidative damage and mitochondrial decay in aging. Proc. Natl Acad. Sci. USA 91, 10771-10778. (doi:10.1073/pnas.91.23.10771)
54. Petros JA et al. 2005 mtDNA mutations increase tumorigenicity in prostate cancer. Proc. Natl Acad. Sci. USA 102, 719-724. (doi:10.1073/pnas. 0408894102)
55. Afanas'ev I. 2010 Signaling and damaging functions of free radicals in aging-free radical theory, hormesis, and TOR. Aging Dis. 1, 75-88.
56. Jacobs HT. 2003 The mitochondrial theory of aging: dead or alive? Aging Cell 2, 11-17. (doi:10.1046/j. 1474-9728.2003.00032.x)
57. Park CB, Larsson NG. 2011 Mitochondrial DNA mutations in disease and aging. J. Cell Biol. 193, 809-818. (doi:10.1083/jcb.201010024)
58. Kujoth GC et al. 2005 Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309, 481-484. (doi:10.1126/ science.1112125)
59. Trifunovic A et al. 2004 Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423. (doi:10.1038/nature02517)
60. Trifunovic A et al. 2005 Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc. Natl Acad. Sci. USA 102, 17993-17998. (doi:10.1073/pnas. 0508886102)
61. Sasaki T, Unno K, Tahara S, Shimada A, Chiba Y, Hoshino M, Kaneko T. 2008 Age-related increase of superoxide generation in the brains of mammals and birds. Aging Cell 7, 459-469. (doi:10.1111/j. 1474-9726.2008.00394.x)
62. Mendoza-Nunez VM, Ruiz-Ramos M, Sanchez- Rodriguez MA, Retana-Ugalde R, Munoz-Sanchez JL. 2007 Aging-related oxidative stress in healthy humans. Tohoku J. Exp. Med. 213, 261-268. (doi:10.1620/tjem.213.261)
63. Miyazawa M, Ishii T, Yasuda K, Noda S, Onouchi H, Hartman PS, Ishii N. 2009 The role of mitochondrial superoxide anion (O2 2) on physiological aging in C57BL/6J mice. J. Radiat. Res. 50, 73-83. (doi:10.1269/jrr.08097)
64. Lund DD, Chu Y, Miller JD, Heistad DD. 2009 Protective effect of extracellular superoxide dismutase on endothelial function during aging. Am. J. Physiol. Heart Circ. Physiol. 296, H1920-H1925. (doi:10.1152/ajpheart.01342.2008)
65. Donato AJ, Eskurza I, Silver AE, Levy AS, Pierce GL, Gates PE, Seals DR. 2007 Direct evidence of endothelial oxidative stress with aging in humans: relation to impaired endothelium-dependent dilation and upregulation of nuclear factor-kB. Circ. Res. 100, 1659-1666. (doi:10.1161/01.RES. 0000269183.13937.e8)
66. Choksi KB, Roberts 2nd LJ, DeFord JH, Rabek JP, Papaconstantinou J. 2007 Lower levels of F2-isoprostanes in serum and livers of long-lived Ames dwarf mice. Biochem. Biophys. Res. Commun. 364, 761-764. (doi:10.1016/j.bbrc.2007.10.100)
67. Jacobson A, Yan C, Gao Q, Rincon-Skinner T, Rivera A, Edwards J, Huang A, Kaley G, Sun D. 2007 Aging enhances pressure-induced arterial superoxide formation. Am. J. Physiol. Heart Circ. Physiol. 293, H1344-H1350. (doi:10.1152/ajpheart. 00413.2007)
68. Lener B, Koziel R, Pircher H, Hutter E, Greussing R, Herndler-Brandstetter D, Hermann M, Unterluggauer H, Jansen-Durr P. 2009 The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem. J. 423, 363-374. (doi:10.1042/BJ20090666)
69. Rodriguez-Manas L et al. 2009 Endothelial dysfunction in aged humans is related with oxidative stress and vascular inflammation. Aging Cell 8, 226-238. (doi:10.1111/j.1474-9726.2009.00466.x)
70. Allen JF. 1996 Separate sexes and the mitochondrial theory of ageing. J. Theor. Biol. 180, 135-140. (doi:10.1006/jtbi.1996.0089)
71. Allen CA, van der Giezen M, Allen JF. 2007 Origin, function and transmission of mitochondria. In Origins of mitochondria and hydrogenosomes (eds W Martin, M Muller), pp. 39-56. Berlin, Heidelberg: Springer.
72. Al Rawi S, Louvet-Vallee S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V. 2011 Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334, 1144-1147. (doi:10.1126/ science.1211878)
73. Deluca SZ, O'Farrell PH. 2013 Barriers to male transmission of mitochondrial DNA in sperm development. Dev. Cell 22, 660-668. (doi:10.1016/ j.devcel.2011.12.021)
74. Sato M, Sato K. 2011 Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334, 1141-1144. (doi:10.1126/science.1210333)
75. Collins AG, Schuchert P, Marques AC, Jankowski T, Medina M, Schierwater B. 2006 Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst. Biol. 55, 97-115. (doi:10.1080/ 10635150500433615)
76. Cartwright P, Halgedahl SL, Hendricks JR, Jarrard RD, Marques AC, Collins AG, Lieberman BS. 2007 Exceptionally preserved jellyfishes from the middle Cambrian. PLoS One 2, e1121. (doi:10.3410/f. 1093897.548834)
77. Ojimi MC, Hidaka M. 2010 Comparison of telomere length among different life cycle stages of the jellyfish Cassiopea andromeda. Mar. Biol. 157, 2279-2287. (doi:10.1007/s00227-010-1495-4)
78. Butterfield NJ. 1997 Plankton ecology and the Proterozoic-Phanerozoic transition. Paleobiology 23, 247-262.
79. Condon RH et al. 2012 Questioning the rise of gelatinous zooplankton in the world's oceans. Bioscience 62, 160-169. (doi:10.1525/bio. 2012.62.2.9)
80. Butterfield NJ. 2000 Bangiomorpha pubescens n. gen, n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/ Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386-404. (doi:10.1666/0094- 8373(2000)026<0386:BPNGNS>2.0.CO;2)
81. Extavour CG, Akam M. 2003 Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869-5884. (doi:10.1242/dev.00804)
82. Morandini AC, Da Silveira FL. 2001 Sexual reproduction of Nausithoe aurea (Scyphozoa, Coronatae) gametogenesis, egg release, embryonic development, and gastrulation. Sci. Mar. 65, 139-149.
83. Dawson MN, Martin LE. 2001 Geographic variation and ecological adaptation in Aurelia (Scyphozoa, Semaeostomeae): some implications from molecular phylogenetics. Hydrobiologia 451, 259-273. (doi:10.1023/A:1011869215330)
84. Lucas CH. 2001 Reproduction and life history strategies of the common jellyfish, Aurelia aurita, in relation to its ambient environment. Hydrobiologia 451, 229-246. (doi:10.1023/A:1011836326717)
85. Shao ZY, Graf S, Chaga OY, Lavrov DV. 2006 Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): a linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381, 92-101. (doi:10.1016/j. gene.2006.06.021)
86. Hirst AG, Lucas CH. 1998 Salinity influences body weight quantification in the scyphomedusa Aurelia aurita: important implications for body weight determination in gelatinous zooplankton. Mar Ecol Prog Ser 165, 259-269. (doi:10.3354/meps165259)
87. Mitchell P. 1979 Keilins respiratory-chain concept and its chemiosmotic consequences. Science 206, 1148-1159. (doi:10.1126/science.388618)
88. Rich P. 2003 The cost of living. Nature 421, 583-583. (doi:10.1038/421583a)
89. Pendergrass W, Wolf N, Poot M. 2004 Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A 61, 162-169. (doi:10.1002/cyto.a.20033)
90. Owusu-Ansah E, Yavari A, Banerjee U. 2008 A protocol for in vivo detection of reactive oxygen species. Protocol Exchange. (doi:10.1038/nprot. 2008.23)
91. de Paula WBM, Agip A-N, Missirlis F, Ashworth R, Vizcay-Barrena G, Lucas C, Allen JF. Submitted. Mitochondrial function in the origin of the female germ line.
92. Hsieh RH, Au HK, Yeh TS, Chang SJ, Cheng YF, Tzeng CR. 2004 Decreased expression of mitochondrial genes in human unfertilized oocytes and arrested embryos. Fertil. Steril. 81(Suppl. 1), 912-918. (doi:10.1016/j.fertnstert. 2003.11.013)
93. Santos TA, Shourbagy SE, John JCS. 2006 Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584-591. (doi:10.1016/j.fertnstert.2005.09.017)
94. Wilding M, Dale B, Marino M, diMatteo L, Alviggi C, Pisaturo ML, Lombardi L, dePlacido G. 2001 Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909-917. (doi:10.1093/humrep/ 16.5.909)
95. Weismann A. 1889 Essays upon heredity, vols 1 and 2. Oxford: The Clarendon Press.
96. Crick F. 1970 Central dogma of molecular biology. Nature 227, 561-563. (doi:10.1038/ 227561a0)
97. Bogorad L. 1975 Evolution of organelles and eukaryotic genomes. Science 188, 891-898. (doi:10.1126/science.1138359)
98. Allen JF, Allen CA. 1999 A mitochondrial model for premature ageing of somatically cloned mammals. IUBMB Life 48, 369-372. (doi:10.1080/713803544)
99. Maynard Smith J. 1966 The theory of evolution, 2nd edn. London: Penguin Books.
100. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, Larsson NG. 2008 Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol. 6, e10. (doi:10.1371/ journal.pbio.0060010)
101. Fan W et al. 2008 A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 319, 958-962. (doi:10.1126/science.1147786)
102. Reynier P, Chretien MF, Savagner F, Larcher G, Rohmer V, Barriere P, Malthiery Y. 1998 Long PCR analysis of human gamete mtDNA suggests defective mitochondrial maintenance in spermatozoa and supports the bottleneck theory for oocytes. Biochem. Biophys. Res. Commun. 252, 373-377. (doi:10.1006/ bbrc.1998.9651)
103. Hadjivasiliou Z, Pomiankowski A, Seymour RM, Lane N. 2012 Selection for mitonuclear co-adaptation could favour the evolution of two sexes. Proc. R. Soc. B 279, 1865-1872. (doi:10.1098/rspb.2011.1871)
104. Lane N. 2011 Mitonuclear match: Optimizing fitness and fertility over generations drives ageing within generations. Bioessays 33, 860-869. (doi:10.1002/ bies.201100051)
105. Zouros E, Ball AO, Saavedra C, Freeman KR. 1994 An unusual type of mitochondrial-DNA inheritance in the blue mussel mytilus. Proc. Natl Acad. Sci. USA 91, 7463-7467. (doi:10.1073/ pnas.91.16.7463)
106. Howard CV, Reed MG. 2010 Unbiased stereology: three-dimensional measurement in microscopy, 2nd edn. Liverpool: QTP Publications.