Extensive paternal mtDNA leakage in natural populations of Drosophila melanogaster

Molecular Ecology

Volumn 22, Issue 8, 2013, Pages 2106-2117

  Nunes, Maria D S ^a,b   Dolezal, Marlies ^a   Schlötterer, Christian ^a  

^a Institut fur Populationsgenetik   (Austria)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Drosophila melanogaster; heteroplasmy; mtDNA diversity; paternal leakage; recombination

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; DROSOPHILA MELANOGASTER; FEMALE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POPULATION; THEORETICAL MODEL;

ANIMALS; DNA, MITOCHONDRIAL; DROSOPHILA MELANOGASTER; FEMALE; GENETIC VARIATION; HAPLOTYPES; MODELS, THEORETICAL; MOLECULAR SEQUENCE DATA; POPULATION; RECOMBINATION, GENETIC;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 84875863526     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12256     Document Type: Article

References (65)

1. Al Rawi S, Louvet-Vallee S, Djeddi A, et al,. (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science, 334, 1144-1147.
2. Altschul SF, Madden TL, Schaffer AA, et al,. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389-3402. (Pubitemid 27359211)
3. Ballard JW, (2000) Comparative genomics of mitochondrial DNA in members of the Drosophila melanogaster subgroup. Journal of Molecular Evolution, 51, 48-63.
4. Barr CM, Neiman M, Taylor DR, (2005) Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytologist, 168, 39-50.
5. Bensasson D, Zhang D, Hartl DL, Hewitt GM, (2001) Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology & Evolution, 16, 314-321. (Pubitemid 32706648)
6. Bruen TC, Philippe H, Bryant D, (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics, 172, 2665-2681.
7. Charlesworth D, Morgan MT, Charlesworth B, (1993) Mutation accumulation in finite outbreeding and inbreeding populations. Genetical Research, 61, 39-56. (Pubitemid 23215490)
8. Ciborowski KL, Consuegra S, Garcia de Leaniz C, et al,. (2007) Rare and fleeting: An example of interspecific recombination in animal mitochondrial DNA. Biology Letters, 3, 554-557.
9. Clement M, Posada D, Crandall KA, (2000) TCS: A computer program to estimate gene genealogies. Molecular Ecology, 9, 1657-1659.
10. Cortese JD, (1999) Rat liver GTP-binding proteins mediate changes in mitochondrial membrane potential and organelle fusion. American Journal of Physiology, 276, C611-C620. (Pubitemid 29157377)
11. 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. (Pubitemid 351171395)
12. D'Aurelio M, Gajewski CD, Lin MT, et al,. (2004) Heterologous mitochondrial DNA recombination in human cells. Human Molecular Genetics, 13, 3171-3179. (Pubitemid 40045269)
13. Dean MD, Ballard KJ, Glass A, Ballard JW, (2003) Influence of two Wolbachia strains on population structure of East African Drosophila simulans. Genetics, 165, 1959-1969. (Pubitemid 38040283)
14. DeLuca SZ, O'Farrell PH, (2012) Barriers to male transmission of mitochondrial DNA in sperm development. Developmental Cell, 22, 660-668.
15. Gantenbein B, Fet V, Gantenbein-Ritter IA, Balloux F, (2005) Evidence for recombination in scorpion mitochondrial DNA (Scorpiones: Buthidae). Proceedings of the Royal Society of London B: Biological Sciences, 272, 697-704. (Pubitemid 41411127)
16. Gyllensten U, Wharton D, Josefsson A, Wilson AC, (1991) Paternal inheritance of mitochondrial DNA in mice. Nature, 352, 255-257. (Pubitemid 21912330)
17. Hale LR, Singh RS, (1986) Extensive variation and heteroplasmy in size of mitochondrial DNA among geographic populations of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 83, 8813-8817.
18. 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.
19. Hedrick P, (2000) Genetics of Populations, 2nd edn. Jones and Bartlett Publishers, Sudbury, Massachusetts.
20. Hiraoka J, Hirao Y, (1988) Fate of sperm tail components after incorporation into the hamster egg. Gamete Research, 19, 369-380.
21. Hudson RR, Kaplan NL, (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics, 111, 147-164. (Pubitemid 16248827)
22. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254-267. (Pubitemid 43100040)
23. 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 of the United States of America, 92, 4542-4546.
24. Kondo R, Satta Y, Matsuura ET, et al,. (1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics, 126, 657-663. (Pubitemid 20372384)
25. Kondo R, Matsuura ET, Chigusa SI, (1992) Further observation of paternal transmission of Drosophila mitochondrial DNA by PCR selective amplification method. Genetical Research, 59, 81-84.
26. Kraytsberg Y, Schwartz M, Brown TA, et al,. (2004) Recombination of human mitochondrial DNA. Science, 304, 981. (Pubitemid 38638088)
27. Kvist L, Martens J, Nazarenko AA, Orell M, (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Molecular Biology and Evolution, 20, 243-247. (Pubitemid 36237382)
28. Ladoukakis ED, Zouros E, (2001) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Molecular Biology and Evolution, 18, 1168-1175. (Pubitemid 32660664)
29. Lakshmipathy U, Campbell C, (1999a) Double strand break rejoining by mammalian mitochondrial extracts. Nucleic Acids Research, 27, 1198-1204. (Pubitemid 29209526)
30. Lakshmipathy U, Campbell C, (1999b) The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Molecular and Cellular Biology, 19, 3869-3876. (Pubitemid 29193846)
31. Lansman RA, Avise JC, Huettel MD, (1983) Critical experimental test of the possibility of "paternal leakage" of mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America, 80, 1969-1971. (Pubitemid 13079215)
32. Librado P, Rozas J, (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
33. Matsuura ET, Fukuda H, Chigusa SI, (1991) Mitochondrial DNA heteroplasmy maintained in natural populations of Drosophila simulans in Reunion. Genetical Research, 57, 123-126.
34. Meusel MS, Moritz RF, (1993) Transfer of paternal mitochondrial DNA during fertilization of honeybee (Apis mellifera L.) eggs. Current Genetics, 24, 539-543. (Pubitemid 24038926)
35. Miller SA, Dykes DD, Polesky HF, (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research, 16, 1215.
36. Newton CR, Graham A, Heptinstall LE, et al,. (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Research, 17, 2503-2516. (Pubitemid 19103235)
37. Nunes MD, Neumeier H, Schlötterer C, (2008a) Contrasting patterns of natural variation in global Drosophila melanogaster populations. Molecular Ecology, 17, 4470-4479.
38. Nunes MD, Nolte V, Schlötterer C, (2008b) Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Molecular Biology and Evolution, 25, 2493-2498.
39. Pearl SA, Welch ME, McCauley DE, (2009) Mitochondrial heteroplasmy and paternal leakage in natural populations of Silene vulgaris, a gynodioecious plant. Molecular Biology and Evolution, 26, 537-545.
40. Piganeau G, Gardner M, Eyre-Walker A, (2004) A broad survey of recombination in animal mitochondria. Molecular Biology and Evolution, 21, 2319-2325. (Pubitemid 39488902)
41. 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. (Pubitemid 18003683)
42. Rand DM, Harrison RG, (1986) Mitochondrial DNA transmission genetics in crickets. Genetics, 114, 955-970.
43. Richardson MF, Weinert LA, Welch JJ, et al,. (2012) Population genomics of the Wolbachia Endosymbiont in Drosophila melanogaster. PLoS Genetics, 8, e1003129.
44. Sato M, Sato K, (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science, 334, 1141-1144.
45. Satta Y, Toyohara N, Ohtaka C, et al,. (1988) Dubious maternal inheritance of mitochondrial DNA in D. simulans and evolution of D. mauritiana. Genetical Research, 52, 1-6.
46. Schwartz M, Vissing J, (2002) Paternal inheritance of mitochondrial DNA. New England Journal of Medicine, 347, 576-580.
47. Sherengul W, Kondo R, Matsuura ET, (2006) Analysis of paternal transmission of mitochondrial DNA in Drosophila. Genes and Genetic Systems, 81, 399-404. (Pubitemid 46232777)
48. 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. (Pubitemid 28087632)
49. Solignac M, Génermont J, Monnerot M, Mounolou J-C, (1984) Genetics of mitochondria in Drosophila: mtDNA inheritance in heteroplasmic strains of D. mauritiana. Molecular Genetics and Genomics: MGG, 197, 183-188.
50. Steinborn R, Zakhartchenko V, Wolf E, Muller M, Brem G, (1998) Non-balanced mix of mitochondrial DNA in cloned cattle produced by cytoplast-blastomere fusion. FEBS Letters, 426, 357-361. (Pubitemid 28218379)
51. Sutovsky P, Moreno RD, Ramalho-Santos J, et al,. (1999) Ubiquitin tag for sperm mitochondria. Nature, 402, 371-372. (Pubitemid 129544815)
52. 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. (Pubitemid 36519787)
53. Takahata N, Maruyama T, (1981) A mathematical-model of extranuclear genes and the genetic-variability maintained in a finite population. Genetical Research, 37, 291-302. (Pubitemid 11091179)
54. Templeton AR, Crandall KA, Sing CF, (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics, 132, 619-633.
55. 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. (Pubitemid 36806830)
56. Thyagarajan B, Padua RA, Campbell C, (1996) Mammalian mitochondria possess homologous DNA recombination activity. Journal of Biological Chemistry, 271, 27536-27543. (Pubitemid 26367317)
57. Townsend JP, Rand DM, (2004) Mitochondrial genome size variation in New World and Old World populations of Drosophila melanogaster. Heredity, 93, 98-103. (Pubitemid 38965203)
58. 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. (Pubitemid 40471406)
59. Ujvari B, Dowton M, Madsen T, (2007) Mitochondrial DNA recombination in a free-ranging Australian lizard. Biology Letters, 3, 189-192. (Pubitemid 351878163)
60. White DJ, Wolff JN, Pierson M, Gemmell NJ, (2008) Revealing the hidden complexities of mtDNA inheritance. Molecular Ecology, 17, 4925-4942.
61. Wolff JN, Gemmell NJ, (2008) Lost in the zygote: The dilution of paternal mtDNA upon fertilization. Heredity (Edinb), 101, 429-434.
62. Wolff JN, Nafisinia M, Sutovsky P, Ballard JWO, (2013) Paternal transmission of mitochondrial DNA as an integral part of mitochondrial inheritance in metapopulations of Drosophila simulans. Heredity, 110, 57-62.
63. Wright S, (1968) Evolution and the Genetics of Populations: A Treatise. University of Chicago Press, Chicago, Illinois.
64. Wu DY, Ugozzoli L, Pal BK, Wallace RB, (1989) Allele-specific enzymatic amplification of beta-globin genomic DNA for diagnosis of sickle cell anemia. Proceedings of the National Academy of Sciences of the United States of America, 86, 2757-2760. (Pubitemid 19112620)
65. Yaffe MP, (1999) The machinery of mitochondrial inheritance and behavior. Science, 283, 1493-1497.