Naturwissenschaften

, Volume 91, Issue 11, pp 505–518

The evolutionary processes of mitochondrial and chloroplast genomes differ from those of nuclear genomes

Review

Abstract

This paper first introduces our present knowledge of the origin of mitochondria and chloroplasts, and the organization and inheritance patterns of their genomes, and then carries on to review the evolutionary processes influencing mitochondrial and chloroplast genomes. The differences in evolutionary phenomena between the nuclear and cytoplasmic genomes are highlighted. It is emphasized that varying inheritance patterns and copy numbers among different types of genomes, and the potential advantage achieved through the transfer of many cytoplasmic genes to the nucleus, have important implications for the evolution of nuclear, mitochondrial and chloroplast genomes. Cytoplasmic genes transferred to the nucleus have joined the more strictly controlled genetic system of the nuclear genome, including also sexual recombination, while genes retained within the cytoplasmic organelles can be involved in selection and drift processes both within and among individuals. Within-individual processes can be either intra- or intercellular. In the case of heteroplasmy, which is attributed to mutations or biparental inheritance, within-individual selection on cytoplasmic DNA may provide a mechanism by which the organism can adapt rapidly. The inheritance of cytoplasmic genomes is not universally maternal. The presence of a range of inheritance patterns indicates that different strategies have been adopted by different organisms. On the other hand, the variability occasionally observed in the inheritance mechanisms of cytoplasmic genomes reduces heritability and increases environmental components in phenotypic features and, consequently, decreases the potential for adaptive evolution.

References

  1. Adoutte A, Beisson J (1972) Evolution of mixed populations of genetically different mitochondria in Paramecium aurelia. Nature 235:393–396Google Scholar
  2. Albert B, Lelandais C, Pla M, Leuret C, Vitart V, Mathieu C, Sihachakr D, Godelle B, De-Paepe R (2003) Amplification of Nicotiana sylvestris mitochondrial subgenomes is under nuclear control and is associated with phenotypic changes. Genetica 117:17–25CrossRefPubMedGoogle Scholar
  3. Allen JF (2003) The function of genomes in bioenergetic organelles. Philos Trans R Soc London B 358:19–38CrossRefGoogle Scholar
  4. Allen JF, Raven JA (1996) Free-radical-induced mutation vs. redox regulation: costs and benefits of genes in organelles. J Mol Evol 42:482–492PubMedGoogle Scholar
  5. Anderson JB, Wickens C, Khan M, Cowen LE, Federspiel N, Jones T, Kohn LM (2001) Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J Bacteriol 183:865–872CrossRefPubMedGoogle Scholar
  6. Archibald JM, Keeling PJ (2002) Recycled plastids: a ‘green movement’ in eukaryotic evolution. Trends Genet 18:577–584CrossRefPubMedGoogle Scholar
  7. Avise JC (1998) The genetic gods: evolution and belief in human affairs. Harvard University Press, Cambridge, Mass.Google Scholar
  8. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744PubMedGoogle Scholar
  9. Behura SK, Sahu SC, Mohan M, Nair S (2001) Wolbachia in the Asian rice gall midge, Orseolia oryzae (Wood-Mason): correlation between host mitotypes and infection status. Insect Mol Biol 10:163–171CrossRefPubMedGoogle Scholar
  10. Bergstrom CT, Pritchard J (1998) Germline bottlenecks and the evolutionary maintenance of mitochondrial genomes. Genetics 149:2135–2146PubMedGoogle Scholar
  11. Bergthorsson U, Adams KL, Thomason B, Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197–201CrossRefPubMedGoogle Scholar
  12. Besnard G, Khadari B, Baradat P, Berville A (2002) Combination of chloroplast and mitochondrial DNA polymorphisms to study cytoplasm genetic differentiation in the olive complex (Olea europaea L.). Theor Appl Genet 105:139–144CrossRefPubMedGoogle Scholar
  13. Birky CW Jr (1973) On the origin of mitochondrial mutants: evidence for intracellular selection of mitochondria in the origin of antibiotic-resistant cells in yeast. Genetics 74:421–432PubMedGoogle Scholar
  14. Birky CW Jr (1991) Evolution and population genetics of organelle genes: mechanisms and models. In: Selander RK, Clark AG, Whittam TS (eds) Evolution at the molecular level. Sinauer, Sunderland, Mass., pp 112–134Google Scholar
  15. Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338PubMedGoogle Scholar
  16. Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148CrossRefPubMedGoogle Scholar
  17. Birky CW Jr, Demko CA, Perlman PS, Strausberg R (1978) Uniparental inheritance of mitochondrial genes in yeast: dependence on input bias of mitochondrial DNA and preliminary investigations of the mechanism. Genetics 89:615–651PubMedGoogle Scholar
  18. Birky CW Jr, 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 121:613–628PubMedGoogle Scholar
  19. Blanchard JL, Lynch M (2000) Organellar genes: why do they end up in the nucleus? Trends Genet 16:315–320CrossRefPubMedGoogle Scholar
  20. Blier PO, Dufresne F, Burton RS (2001) Natural selection and the evolution of mtDNA encoded peptides: evidence for intergenomic co-adaptation. Trends Genet 17:400–406CrossRefPubMedGoogle Scholar
  21. Brewer LR, Friddle R, Noy A, Baldwin E, Martin SS, Corzett M, Balhorn R, Baskin R (2003) Packaging of single DNA molecules by the yeast mitochondrial protein Abf2p. Biophys J 85:2519–2524PubMedGoogle Scholar
  22. Brown DT, Samuels DC, Michael EM, Turnbull DM, Chinnery PF (2001) Random genetic drift determines the level of mutant mtDNA in human primary oocytes. Am J Hum Genet 68:533–536CrossRefPubMedGoogle Scholar
  23. Brums D, Owens JN (2000) Western white pine (Pinus monticola Dougl.) reproduction. II. Fertilization and cytoplasmic inheritance. Sexual Plant Reprod 13:75–84CrossRefGoogle Scholar
  24. Burban C, Petit RJ (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Mol Ecol 12:1487–1495CrossRefPubMedGoogle Scholar
  25. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716CrossRefPubMedGoogle Scholar
  26. Burzynski A, Zbawicka M, Skibirski DOF, Wenne R (2003) Evidence for recombination of mtDNA in the marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20:388–392CrossRefPubMedGoogle Scholar
  27. Cao L, Kenchington E, Zouros E (2004) Differential segregation patterns of sperm mitochondria in embryos of the blue mussel (Mytilus edulis). Genetics 166:883–894PubMedGoogle Scholar
  28. Casane D, Gueride M (2002) Evolution of heteroplasmy at a mitochondrial tandem repeat locus in cultured rabbit cells. Curr Genet 42:66–72CrossRefPubMedGoogle Scholar
  29. Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332–333CrossRefPubMedGoogle Scholar
  30. Chomyn A, Attardi G (2003) MtDNA mutations in aging and apoptosis. Biochem Biophys Res Commun 304:519–529CrossRefPubMedGoogle Scholar
  31. Chong DKX, Chinnappa CC, Yeh FC (1994) Chloroplast DNA inheritance in Stellaria longipes complex (Caryophyllaceae). Theor Appl Genet 88:614–617Google Scholar
  32. 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 228:762–771PubMedGoogle Scholar
  33. Coleman AW (1982) Sex is dangerous in a world of potential symbionts or the basis of selection for uniparental inheritance. J Theor Biol 97:367–369Google Scholar
  34. Crawford AJ (2003) Relative rates of nucleotide substitutions in frogs. J Mol Evol 57:636–641CrossRefPubMedGoogle Scholar
  35. De Benedictis G, Carrieri G, Garasto S, Rose G, Varcasia O, Bonafe M, Franceschi C, Jazwinski SM (2000) Does a retrograde response in human aging and longevity exist? Exp Gerontol 35:795–801CrossRefPubMedGoogle Scholar
  36. De Stordeur E (1997) Nonrandom partition of mitochondria in heteroplasmic Drosophila. Heredity 79:615–623CrossRefGoogle Scholar
  37. Dujon B (1981) Mitochondrial genetics and functions. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeast Saccharomyces. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., pp 505–635Google Scholar
  38. Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304:253–257Google Scholar
  39. Eberhard WG (1980) Evolutionary consequences of intracellular organelle competition. Q Rev Biol 55:231–249CrossRefPubMedGoogle Scholar
  40. Elson JL, Andrews RM, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N (2001) Analysis of European mtDNAs for recombination. Am J Hum Genet 68:145–153CrossRefGoogle Scholar
  41. Elson JL, Turnbull DM, Howell N (2004) Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am J Hum Genet 74:229–238CrossRefPubMedGoogle Scholar
  42. Erickson L, Kemble R (1993) The effect of genotype on pollen transmission of mitochondria in rapeseed (Brassica napus). Sexual Plant Reprod 6:33–39Google Scholar
  43. Eyre-Walker A, Smith NH, Maynard Smith J (1999) Reply to Macaulay et al. (1999): mitochondrial DNA recombination – reasons to panic. Proc R Soc Ser B 266:2041–2042CrossRefGoogle Scholar
  44. Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for Apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426PubMedGoogle Scholar
  45. Fauré S, Noyer JL, Carreel F, Horry JP, Bakry F, Lanaud C (1994) Maternal inheritance of chloroplast genome and paternal inheritance of mitochondrial genome in bananas (Musa acuminata). Curr Genet 25:265–269PubMedGoogle Scholar
  46. Frank SA, Hurst LD (1996) Mitochondria and male disease. Nature 383:224CrossRefGoogle Scholar
  47. Frey JE (1999) Genetic flexibility of plant chloroplasts. Nature 398:115–116CrossRefPubMedGoogle Scholar
  48. Furnier GR, Stine M (1995) Interpopulation differentiation of nuclear and chloroplast loci in white spruce. Can J For Res 25:736–742Google Scholar
  49. Gacser A, Hamari Z, Pfeiffer I, Litter J, Kevei F, Kucsera J (2002) Organization of mitochondrial DNA in the basidiomycetous Dioszegia hungarica (Cryptococcus hungaricus) species. FEMS Microbiol Lett 212:1–6CrossRefPubMedGoogle Scholar
  50. Garrido N, Griparic L, Jokitalo E, Wartiovaara J, Bliek AM van der, Spelbrink JN (2003) Composition and dynamics of human mitochondrial nucleoids. Mol Biol Cell 14:1583–1596CrossRefPubMedGoogle Scholar
  51. Gastony GJ, Yatskievych G (1992) Maternal inheritance of the chloroplast and mitochondrial genomes in cheilanthoid ferns. Am J Bot 79:716–722Google Scholar
  52. Godelle B, Reboud X (1995) Why are organelles uniparentally inherited? Proc R Soc Lond B 259:27–33Google Scholar
  53. Gray MW (1989) Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol 5:25–50PubMedGoogle Scholar
  54. Gray MW, Boer PH (1988) Organization and expression of algal Chlamydomonas reinhardtii mitochondrial DNA. Philos Trans R Soc Lond B 319:135–148Google Scholar
  55. Gray MW, Land BF, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Brossard N, Delage E, Littlejohn TG, Plante I, Rioux P, Saint-Louis D, Zhu Y, Burger G (1998) Genome structure and gene content in protist mitochondrial DNAs. Nucleic Acids Res 26:865–878CrossRefPubMedGoogle Scholar
  56. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481CrossRefPubMedGoogle Scholar
  57. Grun P (1976) Cytoplasmic genetics and evolution. Columbia University Press, New YorkGoogle Scholar
  58. Guillon JM, Raquin C (2000) Maternal inheritance of chloroplasts in the horsetail Equisetum variegatum (Schleich.). Curr Genet 37:53–36CrossRefPubMedGoogle Scholar
  59. Guo FL, Hu SY (1995) Cytological evidence of biparental inheritance of plastids and mitochondria in Pelargonium. Protoplasma 186:201–207Google Scholar
  60. Gurvitz A, Hartig A, Ruis H, Hamilton B, Couet HG de (2002) Preliminary characterization of DML1, an essential Saccharomyces cerevisiae gene related to misato of Drosophila melanogaster. FEMS Yeast Res 2:123–135CrossRefPubMedGoogle Scholar
  61. Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352:255–257CrossRefPubMedGoogle Scholar
  62. Hagelberg E, Goldman N, Lió P, Whelan S, Schiefenhövel W, Glegg JB, Bowden DK (1999) Evidence for mitochondrial DNA recombination in a human population of island Melanesia. Proc R Soc Lond B 266:485–492CrossRefPubMedGoogle Scholar
  63. 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. Mol Biol Evol 19:2261–2264PubMedGoogle Scholar
  64. Hoek AHAM van, Akhmanova AS, Huynen MA, Hackstein JHP (2000) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol Biol Evol 17:202–206PubMedGoogle Scholar
  65. Howe CJ, Barbrook AC, Lockhart PJ (2000) Organelle genes: do they jump or are they pushed? Trends Genet 16:65–66CrossRefPubMedGoogle Scholar
  66. Hu X-S, Ennos RA (1999) Impacts of seed and pollen flow on population genetic structure for plant genomes with three contrasting modes of inheritance. Genetics 152:441–450PubMedGoogle Scholar
  67. Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76CrossRefPubMedGoogle Scholar
  68. Hurst LD, Atlan A, Bengtsson BO (1996) Genetic conflicts. Q Rev Biol 71:317–364CrossRefPubMedGoogle Scholar
  69. Ishida K, Green BR, Cavalier-Smith T (1999) Diversification of a chimaeric algal group, the chlorarachniophytes: phylogeny of nuclear and nucleomorph small-subunit rRNA genes. Mol Biol Evol 16:321–331Google Scholar
  70. Jannotti-Passos LK, Souza CP, Parra JC, Simpson AJG (2001) Biparental mitochondrial DNA inheritance in the parasitic trematode Schistosoma mansoni. J Parasitol 87:79–82PubMedGoogle Scholar
  71. Jenuth JP, Peterson AC, Shoubridge EA (1997) Tissue-specific selection for different mtDNA genotypes in heteroplasmic mice. Nat Genet 16:93–95CrossRefPubMedGoogle Scholar
  72. Kaneda H, Hayashi J-I, Takahama S, Taya C, Fisher Lindahl K, Yonekawa H (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542–4546PubMedGoogle Scholar
  73. Karlberg O, Canbäck B, Kurland CG, Andersson SGE (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17:170–187CrossRefGoogle Scholar
  74. Kato S, Yamaguchi H, Shimamoto Y, Mikami T (2000) The chloroplast genomes of azuki bean and its close relatives: a deletion mutation found in weed azuki bean. Hereditas 132:43–48CrossRefGoogle Scholar
  75. Keys RN, Smith SE, Mogensen HL (1995) Variation in generative cell plastid nucleoids and male fertility in Medicago sativa. Sexual Plant Reprod 8:308–312CrossRefGoogle Scholar
  76. Kobayashi T, Takahara M, Miyagishima S, Kuroiwa H, Sasaki N, Ohta N, Matsuzaki M, Kuroiwa T (2002) Detection and localization of a chloroplast-encoded HU-like protein that organizes chloroplast nucleoids. Plant Cell 14:1579–1589CrossRefPubMedGoogle Scholar
  77. Koji LJ, Cann RL, Martinson JJ, Jorde LB (1998) Mitochondrial and nuclear genetic relationships among Pacific Island and Asian populations. Am J Hum Genet 63:613–624CrossRefPubMedGoogle Scholar
  78. Kondo R, Matsuura ET, Chigusa SI (1992) Further observation of paternal transmission of Drosophila mitochondrial DNA by PCR selective amplification method. Genet Res 59:81–84PubMedGoogle Scholar
  79. Korpelainen H (1999) Genetic maternal effects on human life span through the inheritance of mitochondrial DNA. Hum Hered 49:183–185CrossRefPubMedGoogle Scholar
  80. Kraytsberg Y, Schwartz M, Brown TA, Ebralidse K, Kunz WS, Clayton DA, Vissing J, Khrapko K (2004) Recombination of human mitochondrial DNA. Science 304:981CrossRefGoogle Scholar
  81. Kvist L, Martens J, Nazarenko AA, Orell M (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Mol Biol Evol 20:243–247CrossRefPubMedGoogle Scholar
  82. Ladoukakis ED, Zouros E (2001) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18:1168–1175PubMedGoogle Scholar
  83. Ladoukakis ED, Saavedra C, Magoulas A, Zouros E (2002) Mitochondrial DNA variation in a species with two mitochondrial genomes: the case of Mytilus galloprovincialis from the Atlantic, the Mediterranean and the Black Sea. Mol Ecol 11:755–769CrossRefPubMedGoogle Scholar
  84. Lang-Unnasch N, Reith ME, Munholland J, Barta JR (1998) Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int J Parasitol 28:1743–1754CrossRefPubMedGoogle Scholar
  85. Latta RG, Linhart YB, Mitton JB (2001) Cytonuclear disequilibrium and genetic drift in a natural population of ponderosa pine. Genetics 158:843–850PubMedGoogle Scholar
  86. Lehtinen SK, Hance N, El Meziane A, Juhola MK, Juhola KMI, Karhu R, Spelbrink JN, Holt IJ, Jacobs HT (2000) Genotypic stability, segregation and selection in heteroplasmic human cell lines containing np 3243 mutant mtDNA. Genetics 154:363–380PubMedGoogle Scholar
  87. Lemieux C, Turmel M, Lee RW (1981) Physical evidence for recombination of chloroplast DNA in hybrid progeny of Chlamydomonas eugametos and C. moewusii. Curr Genet 3:97–103Google Scholar
  88. Levings CS III, Brown GG (1989) Molecular biology of plant mitochondria. Cell 56:171–179CrossRefPubMedGoogle Scholar
  89. Lilly JW, Havey MJ, Jackson SA, Jiang J (2001) Cytogenomic analyses reveal the structural plasticity of the chloroplast genome in higher plants. Plant Cell 13:245–254CrossRefPubMedGoogle Scholar
  90. Lin TP, Chuang WJ, Huang SS, Hwang SY (2003) Evidence for the existence of some dissociation in an otherwise strong linkage disequilibrium between mitochondrial and chloroplastic genomes in Cyclobalanopsis glauca. Mol Ecol 12:2661–2668CrossRefPubMedGoogle Scholar
  91. Ling F, Morioka H, Ohtsuka E, Shibata T (2000) A role for MHR1, a gene required for mitochondrial genetic recombination, in the repair of damage spontaneously introduced in yeast mtDNA. Nucleic Acids Res 28:4956–4963CrossRefPubMedGoogle Scholar
  92. Lunt DH, Hyman BC (1997) Animal mitochondrial DNA recombination. Nature 387:247CrossRefPubMedGoogle Scholar
  93. Lyttle TW (1991) Segregation distorters. Annu Rev Genet 25:511–557CrossRefPubMedGoogle Scholar
  94. Magoulas A, Zouros E (1993) Restriction-site heteroplasmy in anchovy (Engraulis encrasicolus) indicates incidental biparental inheritance of mitochondrial DNA. Mol Biol Evol 10:319–325Google Scholar
  95. Mambo E, Gao X, Cohen Y, Guo Z, Talalay P, Sidransky D (2003) Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc Natl Acad Sci USA 100:1838–1843CrossRefGoogle Scholar
  96. Manfredi G, Thyagarajan D, Papadopoulou LC, Pallotti F, Schon EA (1997) The fate of human sperm-derived mtDNA in somatic cells. Am J Hum Genet 61:953–960Google Scholar
  97. Margulis L (1981) Symbiosis in cell evolution. Freeman, San FranciscoGoogle Scholar
  98. Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big hunks. Proc Natl Acad Sci USA 100:8612–8614CrossRefPubMedGoogle Scholar
  99. Martin W, Müller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41CrossRefPubMedGoogle Scholar
  100. Mason PA, Matheson EC, Hall AG, Lightowlers RN (2003) Mismatch repair activity in mammalian mitochondria. Nucleic Acids Res 31:1052–1058CrossRefPubMedGoogle Scholar
  101. Mason RJ, Holsinger KE, Jansen RK (1994) Biparental inheritance of the chloroplast genome in Coreopsis (Asteraceae). J Hered 85:171–173Google Scholar
  102. Masoud SA, Johnson LB, Sorensen EI (1990) High transmission of paternal plastid DNA in alfalfa plants demonstrated by restriction fragment polymorphic analysis. Theor Appl Genet 79:49–55CrossRefGoogle Scholar
  103. May G, Taylor JW (1988) Patterns of mating and mitochondrial DNA inheritance in the agaric basidiomycete Coprinus cinereus. Genetics 118:213–220PubMedGoogle Scholar
  104. May-Panloup P, Chretien MF, Savagner F, Vasseur C, Jean M, Matthiery Y, Reynier P (2003) Increased sperm mitochondrial DNA content in male infertility. Hum Reprod 18:550–556CrossRefPubMedGoogle Scholar
  105. McCauley DE (1994) Contrasting the distribution of chloroplast DNA and allozyme polymorphism among local populations of Silene alba: implications for studies of gene flow in plants. Proc Natl Acad Sci USA 91:8127–8131PubMedGoogle Scholar
  106. McCauley DE (1995) The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends Ecol Evol 10:198–202CrossRefGoogle Scholar
  107. Merriwether DA, Clark AG, Ballinger SW, Schurr TG, Soodyall H, Jenkins T, Sherry ST, Wallace DC (1991) The structure of human mitochondrial variation. J Mol Evol 33:543–555PubMedGoogle Scholar
  108. Meusel MS, Moritz RFA (1993) Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis mellifera L.) eggs. Curr Genet 24:539–543PubMedGoogle Scholar
  109. Mishmar D, Ruiz-Pesini E, Brandon M, Wallace DC (2004) Mitochondrial DNA-like sequences in the nucleus (NUMTs): insights into our African origins and the mechanism of foreign DNA integration. Hum Mutat 23:125–135CrossRefPubMedGoogle Scholar
  110. Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404Google Scholar
  111. Moreira CD, Gmitter FG Jr, Grosser JW, Huang S, Ortega VM, Chase CD (2002) Inheritance of organelle DNA sequences in a Citrus-Poncirus intergeneric cross. J Hered 93:174–178CrossRefPubMedGoogle Scholar
  112. Moriguchi T, Motomura T, Hidaka T, Akihama T, Omura M (1997) Analysis of mitochondrial genomes among Citrus plants produced by the interspecific somatic fusion of seminole tangelo with rough lemon. Plant Cell Rep 16:397–400CrossRefGoogle Scholar
  113. Moriyama EN, Powell JR (1997) Synonymous substitution rates in Drosophila: mitochondrial versus nuclear genes. J Mol Evol 45:378–391PubMedGoogle Scholar
  114. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65CrossRefPubMedGoogle Scholar
  115. Nakazono M, Hirai A (1993) Identification of the entire set of transferred chloroplast DNA sequences in the mitochondrial genome of rice. Mol Gen Genet 236:341–346PubMedGoogle Scholar
  116. Nigro L (1994) Nuclear background affects frequency dynamics of mitochondrial DNA variants in Drosophila simulans. Heredity 72:582–586PubMedGoogle Scholar
  117. Nishimura Y, Misumi O, Kato O, Inada N, Higashiyama T, Momoyama Y, Kuroiwa T (2002) An mt+ gamete-specific nuclease that targets mt- chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev 16:1116–1128CrossRefPubMedGoogle Scholar
  118. Noguchi Y (1932) Studies on the species crosses of Japanese Rhododendron. I. On the crossability between various species and the cotyledon color of F1 seedlings. Jpn J Bot 6:103–124Google Scholar
  119. Norman JE, Gray MW (2001) A complex organization of the gene encoding cytochrome oxidase subunit 1 in the mitochondrial genome of the dinoflagellate, Crypthecodinium cohnii: homologous recombination generates two different cox1 open reading frames. J Mol Evol 53:351–363CrossRefPubMedGoogle Scholar
  120. Oldenburg DJ, Bendich AJ (2004) Most chloroplast DNA of maize seedlings in linear molecules with defined ends and branched forms. J Mol Biol 335:953–970CrossRefPubMedGoogle Scholar
  121. Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354CrossRefPubMedGoogle Scholar
  122. Palmer JD (1997) Organelle genomes: going, going, gone! Science 275:790–791Google Scholar
  123. Palmer JD, Delwiche CF (1998) The origin and evolution of plastids and their genomes. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. II. DNA sequencing. Kluwer, Dordrecht, The Netherlands, pp 375–409Google Scholar
  124. Passamonti M, Scali V (2001) Gender-associated mitochondrial DNA heteroplasmy in the venerid clam Tapes philippinarum (Mollusca Bivalvia). Curr Genet 39:117–124CrossRefPubMedGoogle Scholar
  125. Pont-Kingdon G, Okada NA, MacFarlane JL, Beagley CT, Watkins-Sims CD, Cavalier-Smith T, Clark-Walker GD, Wolstenholme DR (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J Mol Evol 46:419–431PubMedGoogle Scholar
  126. Prina AR (1996) Mutator-induced cytoplasmic mutants in barley: genetic evidence of activation of a putative chloroplast transposon. J Hered 87:385–389Google Scholar
  127. Puomila A, Viitanen T, Savontaus M-L, Nikoskelainen E, Huoponen K (2002) Segregation of the ND4/11778 and the ND1/3460 mutations in four heteroplasmic LHON families. J Neurol Sci 205:41–45CrossRefPubMedGoogle Scholar
  128. Quesada H, Wenne P, Skibinski DOF (1999) Interspecies transfer of female mitochondrial DNA is coupled with role-reversals and departure from neutrality in the mussel Mytilus trossulus. Mol Biol Evol 16:655–665PubMedGoogle Scholar
  129. Rajora OP, Mahon JD (1994) Inheritance of mitochondrial DNA in lentil (Lens culinaris Medik.). Theor Appl Genet 89:206–210Google Scholar
  130. Rajora OP, Mahon JD (1995) Paternal plastid DNA can be inherited in lentil. Theor Appl Genet 90:607–610Google Scholar
  131. Rantanen A, Jansson M, Oldfors A, Larsson NG (2001) Downregulation of Tfam and mtDNA copy number during mammalian spermatogenesis. Mammal Genome 12:787–792CrossRefGoogle Scholar
  132. Reith ME, Munholland J (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Rep 13:333–335Google Scholar
  133. Remacle C, Colin M, Matagne RF (1995) Genetic mapping of mitochondrial markers by recombinational analysis in Chlamydomonas reinhardtii. Mol Gen Genet 249:185–190PubMedGoogle Scholar
  134. Roger AJ (1999) Reconstructing early events in eukaryotic evolution. Am Nat 154:S146–S163CrossRefPubMedGoogle Scholar
  135. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303:223–226CrossRefPubMedGoogle Scholar
  136. Sackton TB, Haney RA, Rand DM (2003) Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57:2315–2325Google Scholar
  137. Saville BJ, Kohli Y, Anderson JB (1998) MtDNA recombination in a natural population. Proc Natl Acad Sci USA 95:1331–1335CrossRefPubMedGoogle Scholar
  138. Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576–580CrossRefPubMedGoogle Scholar
  139. Schwartz M, Vissing J (2003) Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57:2315–2325Google Scholar
  140. Sears BB, Vanwinkle-Swift K (1994) The salvage/turnover/repair (STOR) model for uniparental inheritance in Chlamydomonas: DNA as a source of sustenance. J Hered 85:366–376PubMedGoogle Scholar
  141. Sewell MM, Qiu Y-L, Parks CR, Chase MW (1993) Genetic evidence for trace paternal transmission of plastids in Liriodendron and Magnolia (Magnoliaceae). Am J Bot 80:854–858Google Scholar
  142. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407:81–86CrossRefGoogle Scholar
  143. Shiraishi S, Maeda H, Toda T, Seido K, Sasaki Y (2001) Incomplete paternal inheritance of chloroplast DNA recognized in Chamaecyparis obtusa using an intraspecific polymorphism of the trnD-trnY intergenic spacer region. Theor Appl Genet 102:935–941CrossRefGoogle Scholar
  144. Shitara H, Kaneda H, Sato A, Inoue K, Ogura A, Yonekawa H, Hayashi JI (2000) Selective and continuous elimination of mitochondria microinjected into mouse eggs from spermatids, but not from liver cells, occurs throughout embryogenesis. Genetics 156:1277–1284PubMedGoogle Scholar
  145. Shore JS, Triassi M (1998) Paternally biased cpDNA inheritance in Turnera ulmifolia (Turneraceae). Am J Bot 85:328–332Google Scholar
  146. Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schönfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C (2003) The proteome of Saccharomyces cerevisiae mitochondria. Proc Natl Acad Sci USA 100:13207–13212CrossRefPubMedGoogle Scholar
  147. Sinclair WT, Morman JD, Ennos RA (1998) Multiple origins for Scots pine (Pinus sylvestris L.) in Scotland: evidence from mitochondrial DNA variation. Heredity 80:233–240CrossRefGoogle Scholar
  148. Skibinski DOF, Gallagher C, Quesada H (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 68:195–213CrossRefGoogle Scholar
  149. Slade RW, Moritz C, Hoelzel AR, Burton HR (1998) Molecular population genetics of the Southern elephant seal Mirounga leonina. Genetics 149:1945–1957PubMedGoogle Scholar
  150. Soliman K, Fedak G, Allard RW (1987) Inheritance of organelle DNA in barley and Hordeum × secale intergeneric hybrids. Genome 29:867–872Google Scholar
  151. Song BH, Wang XQ, Wang XR, Ding KY, Hong DY (2003) Cytoplasmic composition in Pinus densata and population establishment of the diploid hybrid pine. Mol Ecol 12:2995–3001CrossRefPubMedGoogle Scholar
  152. Staedler T, Delph LF (2002) Ancient mitochondrial haplotypes and evidence for intragenic recombination in a gynodioecious plant. Proc Natl Acad Sci USA 99:11730–11735CrossRefPubMedGoogle Scholar
  153. Suomalainen A, Kaukonen J (2001) Diseases caused by nuclear genes affecting mtDNA stability. Am J Med Genet 105:53–61CrossRefPubMedGoogle Scholar
  154. Sutovsky P, Moreno RD, Ramalho SJ, Dominko T, Simerly C, Schatten G (2000) Ubiquinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63:582–590PubMedGoogle Scholar
  155. Takano H (2000) Intimate relationship between mtDNA, plasmids, and the fusion of mitochondria. J Plant Res 113:223–229Google Scholar
  156. Takeda K, Akagi S, Kaneyama K, Kojima T, Takahashi S, Imai H, Yamanaka M, Onishi A, Hanada H (2003) Proliferation of donor mitochondrial DNA in nuclear transfer calves (Bos taurus) derived from cumulus cells. Mol Reprod Dev 64:429–437CrossRefPubMedGoogle Scholar
  157. Testolin R, Cipriani G (1997) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in the genus Actinidia. Theor Appl Genet 94:897–903CrossRefGoogle Scholar
  158. Toth B, Hamari Z, Ferenczy L, Varga J, Kevei F (1998) Recombination of mitochondrial DNA without selection pressure among compatible strains of the Aspergillus niger species aggregate. Curr Genet 33:199–205CrossRefPubMedGoogle Scholar
  159. Tomaru N, Takahashi M, Tsumura Y, Takahashi M, Ohba K (1998) Intraspecific variation and phylogeographic patterns of Fagus crenata (Fagaceae) mitochondrial DNA. Am J Bot 85:629–636Google Scholar
  160. Tomaska L, Nosek J, Makhov AM, Pastorakova A, Griffith JD (2000) Extragenomic double-stranded DNA circles in yeast with linear mitochondrial genomes: potential involvement in telomere maintenance. Nucleic Acids Res 28:4479–4487CrossRefPubMedGoogle Scholar
  161. Tovar J, León-Avila G, Sánchez L, Sutak R, Tachezy J, Giezen M van der, Hernández M, Müller M, Lucocq JM (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176CrossRefPubMedGoogle Scholar
  162. Turmel M, Mercier JP, Cote MJ (1993) Group I introns interrupt the chloroplast psaB and psbC and the mitochondrial rrnL gene in Chlamydomonas. Nucleic Acids Res 21:5242–5250PubMedGoogle Scholar
  163. Turner C, Killoran C, Thomas NST, Rosenberg M, Chuzhanova NA, Johnston J, Kemel Y, Cooper DN, Biesecker LG (2003) Human genetic disease caused by de novo mitochondrial-nuclear DNA transfer. Hum Genet 112:303–309PubMedGoogle Scholar
  164. Vellai T, Takacs K, Vida G (1998) A new aspect to the origin and evolution of eukaryotes. J Mol Evol 46:499–507PubMedGoogle Scholar
  165. Wallace DC (1999) Mitochondrial diseases in man and mouse. Science 283:1482–1488Google Scholar
  166. Wei YH, Lee HC (2002) Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp Biol Med 227:671–682Google Scholar
  167. Weigel R, Wolf M, Hesemann CU (1995) Mitochondrial DNA variation in plants regenerated from embryogenic callus cultures of CMS triticale. Theor Appl Genet 91:1237–1241CrossRefGoogle Scholar
  168. Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869CrossRefPubMedGoogle Scholar
  169. Wilson RJ, Denny PW, Preiser PR, Rangachari K, Roberts K, Roy A, Whyte A, Strath M, Moore DJ, Moore PW, Williamson DH (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261:155–172CrossRefPubMedGoogle Scholar
  170. Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12:885–893PubMedGoogle Scholar
  171. Yan Z, Xu J (2003) Mitochondria are inherited from the MATα parent in crosses of the basidiomycete fungus Cryptococcus neoformans. Genetics 163:1315–1325PubMedGoogle Scholar
  172. Yang TW, Yang YA, Xiong Z (2000) Paternal inheritance of chloroplast DNA in interspecific hybrids in the genus Larrea (Zygophyllaceae) Am J Bot 87:1452–1458Google Scholar
  173. Zhang Z, Green BR, Cavalier-Smith T (2000) Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J Mol Evol 51:26–40PubMedGoogle Scholar
  174. Zheng D, Nielsen BL, Daniell H (1997) A 7.5-kbp region of the maize (T cytoplasm) mitochondrial genome contains a chloroplast-like trnI (CAT) pseudo gene and many short segments homologous to chloroplast and other known genes. Curr Genet 32:125–131CrossRefPubMedGoogle Scholar
  175. Zouros E, Ball AD, Saavedra C, Freeman KR (1994) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91:7463–7467PubMedGoogle Scholar

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© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Applied BiologyUniversity of HelsinkiHelsinkiFinland

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