Doubly uniparental inheritance: Two mitochondrial genomes, one precious model for organelle DNA inheritance and evolution

DNA and Cell Biology

Volumn 28, Issue 2, 2009, Pages 79-89

  Passamonti, Marco ^a   Ghiselli, Fabrizio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

AGING; APOPTOSIS; BIVALVE; CELL AGING; CELL DIFFERENTIATION; CELL MATURATION; CELL ORGANELLE; CLINICAL RESEARCH; DEVELOPMENTAL BIOLOGY; DNA RECOMBINATION; EUKARYOTE; EXTRACHROMOSOMAL INHERITANCE; FERTILIZATION; GENOME; HERITABILITY; METABOLIC REGULATION; MITOCHONDRIAL GENOME; MITOCHONDRION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROGENY; REPRODUCTION; REVIEW; SEX DETERMINATION; SEXUAL DEVELOPMENT; SEXUAL TRANSMISSION; UBIQUITINATION;

ANIMALS; EVOLUTION, MOLECULAR; FEMALE; GENOME, MITOCHONDRIAL; HUMANS; MALE; MITOCHONDRIA; MODELS, GENETIC; MOLLUSCA; SEX DETERMINATION (GENETICS);

BIVALVIA; EUKARYOTA; METAZOA; MOLLUSCA;

EID: 59949100674     PISSN: 10445498     EISSN: None     Source Type: Journal    
DOI: 10.1089/dna.2008.0807     Document Type: Review

References (89)

1. Amikura, R., Kashikawa, M., Nakamura, A., and Kobayashi, S. (2001). Presence of mitochondria-type ribosomes outside mitochondria in germ plasm of Drosophila embryos. Proc Natl Acad Sci USA 98, 9133-9138.
2. Andersson, S.G., Zomorodipour, A., Andersson, J.O., Sicheritz-Ponten, T., Alsmark, U.C., Podowski, R.M., et al. (1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133-140.
3. Arctander, P. (1999). Mitochondrial recombination? Science 284, 2090-2091.
4. Awadalla, P., Eyre-Walker, A., and Smith, J.M. (1999). Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science 286, 2524-2525.
5. Bazinet, C. (2004). Endosymbiotic origins of sex. Bioessays 26, 558-566.
6. Bazinet, C., and Rollins, J.E. (2003). Rickettsia-like mitochondrial motility in Drosophila spermiogenesis. Evol Dev 5, 379-385.
7. Birky, C.W., Jr. (1995). Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92, 11331-11338.
8. Birky, C.W., Jr. (2001). The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35, 125-148.
9. Boore, J.L. (1999). Animal mitochondrial genomes. Nucleic Acids Res 27, 1767-1780.
10. Borras, C., Sastre, J., Garcia-Sala, D., Lloret, A., Pallardo, F.V., and Vina, J. (2003). Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34, 546-552.
11. Breton, S., Beaupre, H.D., Stewart, D.T., Hoeh, W.R., and Blier, P.U. (2007). The unusual systemof doubly uniparental inheritance of mtDNA: isn't one enough? Trends Genet 23, 465-474.
12. Breton, S., Burger, G., Stewart, D.T., and Blier, P.U. (2006). Comparative analysis of gender-associated complete mitochondrial genomes in marine mussels (Mytilus spp.). Genetics 172, 1107-1119.
13. Brookes, P.S., Levonen, A.L., Shiva, S., Sarti, P., and Darley-Usmar, V.M. (2002). Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med 33, 755-764.
14. Burzynski, A., Zbawicka, M., Skibinski, D.O., and Wenne, R. (2003). Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20, 388-392.
15. Cao, L., Kenchington, E., and Zouros, E. (2004). Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166, 883-894.
16. Chakrabarti, R., Walker, J.M., Chapman, E.G., Shepardson, S.P., Trdan, R.J., Curole, J.P., et al. (2007). Reproductive function for a C-terminus extended, male-transmitted cytochrome c oxidase subunit II protein expressed in both spermatozoa and eggs. FEBS Lett 581, 5213-5219.
17. Chakrabarti, R., Walker, J.M., Stewart, D.T., Trdan, R.J., Vijayaraghavan, S., Curole, J.P., et al. (2006). Presence of a unique male-specific extension of C-terminus to the cytochrome c oxidase subunit II protein coded by the male-transmitted mitochondrial genome of Venustaconcha ellipsiformis (Bivalvia: Unionoidea). FEBS Lett 580, 862-866.
18. Cogswell, A.T., Kenchington, E.L., and Zouros, E. (2006). Segregation of sperm mitochondria in two- and four-cell embryos of the blue mussel Mytilus edulis: implications for the mechanism of doubly uniparental inheritance of mitochondrial DNA. Genome 49, 799-807.
19. Cosmides, L.M., and Tooby, J. (1981). Cytoplasmic inheritance and intragenomic conflict. J Theor Biol 89, 83-129.
20. Curole, J.P., and Kocher, T.D. (2002). Ancient sex-specific extension of the cytochrome c oxidase II gene in bivalves and the fidelity of doubly-uniparental inheritance. Mol Biol Evol 19, 1323-1328.
21. Curole, J.P., and Kocher, T.D. (2005). Evolution of a unique mitotype-specific protein-coding extension of the cytochrome c oxidase II gene in freshwater mussels (Bivalvia: Unionoida). J Mol Evol 61, 381-389.
22. Dalziel, A.C., and Stewart, D.T. (2002). Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae). Genome 45, 348-355.
23. Ding, D., and Lipshitz, H.D. (1993). A molecular screen for polar-localised maternal RNAs in the early embryo of Drosophila. Zygote 1, 257-271.
24. Ebbert, M.A. (1993). Endosymbiotic sex ratio distorters in insects and mites. In Evolution and Diversity of Sex Ratio in Insects and Mites. D.L. Wrensh and M.A. Ebbert, eds. (Chapman Hall, New York), pp. 150-191.
25. Elson, J.L., Andrews, R.M., Chinnery, P.F., Lightowlers, R.N., Turnbull, D.M., and Howell, N. (2001). Analysis of European mtDNAs for recombination. Am J Hum Genet 68, 145-153.
26. Everett, E.M., Williams, P.J., Gibson, G., and Stewart, D.T. (2004). Mitochondrial DNA polymorphisms and sperm motility in Mytilus edulis (Bivalvia: Mytilidae). J Exp Zoolog A Comp Exp Biol 301, 906-910.
27. Eyre-Walker, A. (1999). Evidence of selection on silent site base composition in mammals: potential implications for the evolution of isochores and junk DNA. Genetics 152, 675-683.
28. Garrido-Ramos, M.S., Stewart, D.T., Sutherland, B.W., and Zouros, E. (1998). The distribution of male-transmitted and female-transmitted mitochondrial DNA types in somatic tissues of blue mussels: implications for the operation of doubly uniparental inheritance of Mitochondrial DNA. Genome 41, 818-824.
29. Gillham, N.W. (1994). Transmission and compatibility of organelle genomes. In Orgenelle Genes and Genomes. (Oxford University Press, New York), pp. 147-268.
30. Gray, M.W., Burger, G., and Lang, B.F. (1999). Mitochondrial evolution. Science 283, 1476-1481.
31. Gyllensten, U., Wharton, D., Josefsson, A., and Wilson, A.C. (1991). Paternal inheritance of mitochondrial DNA in mice. Nature 352, 255-257.
32. Hagelberg, E., Goldman, N., Lio, P., Whelan, S., Schiefenhovel, W., Clegg, J.B., et al. (1999). Evidence for mitochondrial DNA recombination in a human population of island Melanesia. Proc Biol Sci 266, 485-492.
33. Hoeh, W.R., Stewart, D.T., Sutherland, B.W., and Zouros, E. (1996). Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca: Bivalvia). Mol Biol Evol 13, 418-421.
34. Hoekstra, R.F. (1987). The evolution of sexes. Experientia Suppl 55, 59-91.
35. Hoffmann, R.J., Boore, J.L., and Brown, W.M. (1992). A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics 131, 397-412.
36. Hurst, L.D. (1992). Intragenomic conflict as an evolutionary force. Proc Royal Soc Lond B 248, 135-140.
37. Hurst, L.D., and Hamilton, W.D. (1992). Cytoplasmic fusion and the nature of sexes. Proc Royal Soc Lond B 247, 189-194.
38. Hurst, G.D.D., Hurst, L.D., and Majerus, M.E.N. (1997). Cytoplasmic sex-ratio distorters. In Influential Passengers: Inherited Microorganisms and Invertebrate Reproduction. S.L. O'Neil, A.A. Hoffmann, and J.H. Werren, eds. (Oxford University Press, UK), pp. 125-154.
39. Hurst, G.D., and Werren, J.H. (2001). The role of selfish genetic elements in eukaryotic evolution. Nat Rev Genet 2, 597-606.
40. Ikenishi, K. (1998). Germ plasm in Caenorhabditis elegans, Drosophila and Xenopus. Dev Growth Differ 40, 1-10.
41. Ingman, M., Kaessmann, H., Paabo, S., and Gyllensten, U. (2000). Mitochondrial genome variation and the origin of modern humans. Nature 408, 708-713.
42. Jha, M., Côté, J., Hoeh, W.R., Blier, P.U., and Stewart, D.T. (2007). Sperm motility in Mytilus edulis in relation to mitochondrial DNA polymorphism: implications for the evolution of doubly uniparental inheritance in bivalves. Evolution 62, 99-106.
43. Kajander, O.A., Rovio, A.T., Majamaa, K., Poulton, J., Spelbrink, J.N., Holt, I.J., et al. (2000). Human mtDNA sublimons resemble rearranged mitochondrial genomes found in pathological states. Hum Mol Genet 9, 2821-2835.
44. Kaneda, H., Hayashi, J., Takahama, S., Taya, C., Lindahl, K.F., and Yonekawa, H. (1995). Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92, 4542-4546.
45. Kenchington, E., MacDonald, B., Cao, L., Tsagkarakis, D., and Zouros, E. (2002). Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 161, 1579-1588.
46. Kivisild, T., Villems, R., Jorde, L.B., Bamshad, M., Kumar, S., Hedrick, P., et al. (2000). Questioning evidence for recombination in human mitochondrial DNA. Science 288, 1931a.
47. Kloc, M., Bilinski, S., and Etkin, L.D. (2004). The Balbiani body and germ cell determinants: 150 years later. Curr Top Dev Biol 59, 1-36.
48. Kobayashi, S., Amikura, R., and Mukai, M. (1998). Localization of mitochondrial large ribosomal RNA in germ plasm of Xenopus embryos. Curr Biol 8, 1117-1120.
49. Kobayashi, S., Amikura, R., and Okada, M. (1993). Presence of mitochondrial large ribosomal RNA outside mitochondria in germ plasm of Drosophila melanogaster. Science 260, 1521-1524.
50. Kobayashi, S., and Okada, M. (1989). Restoration of pole-cell-forming ability to u.v.-irradiated Drosophila embryos by injection of mitochondrial lrRNA. Development 107, 733-742.
51. Ladoukakis, E.D., and Zouros, E. (2001a). Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18, 1168-1175.
52. Ladoukakis, E.D., and Zouros, E. (2001b). Recombination in animal mitochondrial DNA: evidence from published sequences. Mol Biol Evol 18, 2127-2131.
53. Lenaz, G. (1998). Role of mitochondria in oxidative stress and ageing. Biochim Biophys Acta 1366, 53-67.
54. Liu, H.P., Mitton, J.B., and Wu, S.K. (1996). Paternal mitochondrial DNA differentiation far exceeds maternal DNA and allozyme differentiation in the freshwater mussel, Anodonta grandis grandis. Evolution 50, 952-957.
55. McBride, H.M., Neuspiel, M., and Wasiak, S. (2006). Mitochondria: more than just a powerhouse. Curr Biol 16, R551-R560.
56. Merriweather, D.A., and Kaestle, F.A. (1999). Mitochondrial recombination? (continued). Science 285, 837.
57. Obata, M., Kamiya, C., Kawamura, K., and Komaru, A. (2006). Sperm mitochondrial DNA transmission to both male and female offspring in the blue mussel Mytilus galloprovincialis. Dev Growth Differ 48, 253-261.
58. Obata, M., and Komaru, A. (2005). Specific location of sperm mitochondria in mussel Mytilus galloprovincialis zygotes stained by MitoTracker. Dev Growth Differ 47, 255-263.
59. Obata, M., Shimizu, M., Sano, N., and Komaru, A. (2008). Maternal Inheritance of Mitochondrial DNA (mtDNA) in the Pacific oyster (Crassostrea gigas): a preliminary study using mtDNA sequence analysis with evidence of random distribution of MitoTracker-stained sperm mitochondria in fertilized eggs. Zoolog Sci 25, 248-254.
60. Ohta, T. (1992). The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst 23, 263-286.
61. Partridge, L., and Hurst, L.D. (1998). Sex and conflict. Science 281, 2003-2008.
62. Passamonti, M. (2007). An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca Bivalvia). BMC Evol Biol 7 Suppl 2, S7, 1-11.
63. Passamonti, M., Boore, J.L., and Scali, V. (2003). Molecular evolution and recombination in gender-associated mitochondrial DNAs of the Manila clam Tapes philippinarum. Genetics 164, 603-611.
64. Quesada, H., Warren, M., and Skibinski, D.O. (1998). Nonneutral evolution and differential mutation rate of gender-associated mitochondrial DNA lineages in the marine mussel Mytilus. Genetics 149, 1511-1526.
65. Randerson, J.P., and Hurst, L.D. (1999). Small sperm, uniparental inheritance and selfish cytoplasmic elements: a comparison of two models. J Evol Biol 12, 1110-1124.
66. Rawson, P.D., Secor, C.L., and Hilbish, T.J. (1996). The effects of natural hybridization on the regulation of doubly uniparental mtDNA inheritance in blue mussels (Mytilus spp.). Genetics 144, 241-248.
67. Reunov, A., Isaeva, V., Au, D., and Wu, R. (2000). Nuage constituents arising from mitochondria: is it possible? Dev Growth Differ 42, 139-143.
68. Rokas, A., Ladoukakis, E.D., and Zouros, E. (2003). Animal mitochondrial DNA recombination revisited. Trends Ecol Evol 18, 411-417.
69. Saavedra, C., Reyero, M.I., and Zouros, E. (1997). Male-dependent doubly uniparental inheritance of mitochondrial DNA and female-dependent sex-ratio in the mussel Mytilus galloprovincialis. Genetics 145, 1073-1082.
70. Saavedra, C., Stewart, D.T., Stanwood, R.R., and Zouros, E. (1996). Species-specific segregation of gender-associated mitochondrial DNA types in an area where two mussel species (Mytilus edulis and M. trossulus) hybridize. Genetics 143, 1359-1367.
71. Schapira, A.H. (2006). Mitochondrial disease. Lancet 368, 70-82.
72. Shitara, H., Hayashi, J.I., Takahama, S., Kaneda, H., and 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.
73. Sicheritz-Ponten, T., Kurland, C.G., and Andersson, S.G. (1998). A phylogenetic analysis of the cytochrome b and cytochrome c oxidase I genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim Biophys Acta 1365, 545-551.
74. Skibinski, D.O.F., Gallagher, C., and Beynon, C.M. (1994a). Mitochondrial DNA inheritance. Nature 368, 817-818.
75. Skibinski, D.O.F., Gallagher, C., and Beynon, C.M. (1994b). Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138, 801-809.
76. Skibinski, D.O.F., Gallagher, C., and Beynon, C.M. (1999). On the roles of selection, mutation and drift in the evolution of mitochondrial DNA diversity in British Mytilus edulis (Mytilidae; Mollusca) populations. Biol J Linn Soc 68, 195-213.
77. Stewart, D.T., Saavedra, C., Stanwood, R.R., Ball, A.O., and Zouros, E. (1995). Male and female mitochondrial DNA lineages in the blue mussel (Mytilus edulis) species group. Mol Biol Evol 12, 735-747.
78. Sutovsky, P., Moreno, R.D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature 402, 371-372.
79. Sutovsky, P., Moreno, R.D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (2000). Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63, 582-590.
80. Theologidis, I., Fodelianakis, S., Gaspar, M.B., and Zouros, E. (2008). Doubly uniparental inheritance (DUI) of mitochondrial DNA in Donax trunculus (Bivalvia: Donacidae) and the problem of its sporadic detection in Bivalvia. Evol Int J Org Evol 62, 959-970.
81. Thyagarajan, B., Padua, R.A., and Campbell, C. (1996). Mammalian mitochondria possess homologous DNA recombination activity. J Biol Chem 271, 27536-27543.
82. Van Blerkom, J., and Davis, P. (2007). Mitochondrial signaling and fertilization. Mol Hum Reprod 13, 759-770.
83. Venetis, C., Theologidis, I., Zouros, E., and Rodakis, G.C. (2006). No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc Biol Sci 273, 2483-2489.
84. Wang, X. (2001). The expanding role of mitochondria in apoptosis. Genes Dev 15, 2922-2933.
85. Werren, J.H., and Beukeboom, L.W. (1998). Sex determination, sex ratios and genetic conflict. Annu Rev Ecol Syst 29, 233-261.
86. Yaffe, M.P. (1999). Dynamic mitochondria. Nat Cell Biol 1, E149-E150.
87. Zouros, E. (2000). The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75, 313-318.
88. Zouros, E., Ball, A.O., Saavedra, C., and Freeman, K.R. (1994a). Mitochondrial DNA inheritance. Nature 368, 818.
89. Zouros, E., Oberhauser Ball, A., Saavedra, C., and Freeman, K.R. (1994b). An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91, 7463-7467.