Advertisement

pp 1-25 | Cite as

Doubly Uniparental Inheritance of mtDNA: An Unappreciated Defiance of a General Rule

  • Eleftherios ZourosEmail author
  • George C. Rodakis
Chapter
Part of the Advances in Anatomy, Embryology and Cell Biology book series

Abstract

We recount the basic observations about doubly uniparental inheritance (DUI) of mtDNA in bivalvian mollusks with an emphasis on those that were obtained from work in Mytilus and appeared after the review by Zouros (Evol Biol 40:1–31, 2013). Using this information, we present a new model about DUI that is a revised version of previously suggested models. The model can be summarized as follows. A Mytilus female either provides its eggs with the “masculinizing” factor S and the “sperm mitochondria binding” factor Z, or it does not. This property of the female is determined by two nuclear genes, S and Z, that are always in the on/on or the off/off phase. In fertilized eggs without factors S and Z the embryo develops into a female and the sperm mitochondria are randomly dispersed among cells following development. In fertilized eggs with factors S and Z, the first factor causes the cell to become eventually sperm and the second causes the sperm mitochondria to aggregate and anchor to the nuclear membrane by binding to a specific motif of the sperm-derived mtDNA. Factors S and Z are continuously co-synthesized and co-localized in the cell line from the egg to the sperm. The sperm mitochondria of the aggregate escape the mechanism that eliminates the cell’s mitochondria before the formation of the sperm. The rescued mitochondria are subsequently packed into five mega-mitochondria in the sperm and are delivered in the egg.

Keywords

Blue mussel Doubly uniparental inheritance Mitochondrial DNA inheritance Mytilus 

Notes

Acknowledgment

We thank Dr. M. Ladoukakis for offering helpful comments on an earlier version of the paper.

References

  1. Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates Inc., Sunderland, MAGoogle Scholar
  2. Avise JC, Lansman RA, Shade RO (1979) The use of restriction endonucleases to measure mitochondria1 DNA sequence relatedness in natural populations. I. Population structure and evolution in the genus Peromyscus. Genetics 92:279–295Google Scholar
  3. Breton S, Doucet-Beaupre H, Stewart DT, Hoeh WR (2007) The unusual system of doubly uniparental inheritance of mtDNA: isn’t one enough? Trends Genet 23:465–474Google Scholar
  4. Breton S, Doucet-Beaupre H, Stewart DT, Piontkivska H, Karmakar M, Bogan AE, Blier PU, Hoeh WR (2009) Comparative mitochondrial genomics of fresh water mussels (Bivalvia:Unionoida) with doubly uniparental inheritance of mtDNA: gender-specific open reading frames and putative origins of replication. Genetics 183:1575–1589Google Scholar
  5. Breton S, Ghiselli F, Passamonti M, Stewart DT, Hoeh WR (2011a) Evidence for a fourteenth mtDNA-encoded protein in female-transmitted mtDNA of marine mussels (Bivalvia: Mytilidae). PLoS One 6:e19365Google Scholar
  6. Breton S, Stewart DT, Shepardson S, Trdan RJ, Bogan AE, Chapman EG, Ruminas AJ, Piontkivska H, Hoeh WR (2011b) Novel protein genes in animal mtDNA: a new sex determination system in freshwater mussels (Bivalvia: Unionoida)? Mol Biol Evol 28:1645–1659Google Scholar
  7. Burzynski A, Zbawicka M, Skibinski DOF, Wenne R (2003) Evidence of recombination of mtDNA in marine mussel Mytilus trossulus from the Baltic. Mol Biol Evol 20:388–392Google Scholar
  8. Cao L, Kenchington EL, Zouros E (2004a) Differential segregation patterns of sperm mitochondria in embryos of the Blue Mussel (Mytilus edulis). Genetics 166:883–894Google Scholar
  9. Cao L, Kenchington EL, Zouros E, Rodakis GC (2004b) Evidence that the large noncoding sequence is the main control region of maternally and paternally transmitted mitochondrial genomes of the marine mussel (Mytilus spp.). Genetics 167:835–850Google Scholar
  10. Chatzoglou E, Kyriakou E, Zouros E, Rodakis GC (2013) The mRNAs of maternally and paternally inherited mtDNAs of the mussel Mytilus galloprovincialis: start/end points and polycistronic transcripts. Gene 520:156–165Google Scholar
  11. Dalziel AC, Stewart DT (2002) Tissue-specific expression of male-transmitted mitochondrial DNA and its implications for rates of molecular evolution in Mytilus mussels (Bivalvia: Mytilidae). Genome 45:348–355Google Scholar
  12. DeLuca SZ, O’Farrell PH (2012) Barriers to male transmission of mitochondrial DNA in sperm development. Dev Cell 22:660–668Google Scholar
  13. Doucet-Beaupre H, Breton S, Chapman EG, Blier PU, Stewart DT, Hoeh WR (2010) Mitochondrial phylogenetics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA. BMC Evol Biol 10:50Google Scholar
  14. Fisher C, Skibinski DOF (1990) Sex-biased mitochondrial heteroplasmy in the marine mussel Mytilus. Proc R Soc Lond B Biol Sci 242:149–156Google Scholar
  15. Garrido-Ramos MA, Stewart DT, Sutherland BW, 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 41:818–824Google Scholar
  16. Ghiselli F, Milani L, Passamonti M (2011) Strict sex-specific mtDNA segregation in the germ line of the DUI species Venerupis philippinarum (Bivalvia: Veneridae). Mol Biol Evol 28:949–961Google Scholar
  17. Ghiselli F, Milani L, Chang PL, Hedgecock D, Davis JP, Nuzhdin SV, Passamonti M (2012) De novo assembly of the manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination. Mol Biol Evol 29:771–786Google Scholar
  18. Gusman A, Lecomte S, Stewart DT, Passamonti M, Breton S (2016) Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA. PeerJ 4:e2760Google Scholar
  19. Hayashi JI, Yonekawa H, Gotoh O, Watanabe J, Tagashira Y (1978) Strictly maternal inheritance of rat mitochondrial DNA. Biochem Biophys Res Commun 83:1032–1038Google Scholar
  20. Hoeh WR, Blakey KH, Brown WM (1991) Heteroplasmy suggests limited biparental inheritance in Mytilus mitochondrial-DNA. Science 251:1488–1490Google Scholar
  21. Hoeh WR, Stewart DT, Sutherland BW, Zouros E (1996) Cytochrome c oxidase sequence comparisons suggest an unusually high rate of mitochondrial DNA evolution in Mytilus (Mollusca:Bivalvia). Mol Biol Evol 13:418–421Google Scholar
  22. Hutchison CA, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538Google Scholar
  23. Kenchington EL, MacDonald B, Cao L, Tsagkarakis D, Zouros E (2002) Genetics of mother-dependent sex ratio in blue mussels (Mytilus spp.) and implications for doubly uniparental inheritance of mitochondrial DNA. Genetics 161:1579–1588Google Scholar
  24. Kenchington EL, Hamilton L, Cogswell A, Zouros E (2009) Paternal mtDNA and maleness are co-inherited but not causally linked in mytilid Mussels. PLoS One 4:e6976Google Scholar
  25. Kiyomoto M, Komaru A, Scarpa J, Wada KT, Danton E et al (1996) Abnormal gametogenesis, male dominant sex ratio, and Sertoli cell morphology in induced triploid mussels, Mytilus galloprovincialis. Zoolog Sci 13:393–402Google Scholar
  26. Kyriakou E, Zouros E, Rodakis GC (2010) The atypical presence of the paternal mitochondrial DNA in somatic tissues of male and female individuals of the blue mussel species Mytilus galloprovincialis. BMC Res Notes 3:222Google Scholar
  27. Kyriakou E, Kravariti L, Zouros E, Rodakis GC (2013) Sex-specific mtDNA-protein interactions in a system of obligatory biparental inheritance and the exceptional role of perinuclear mitochondria. SW03S14-32Google Scholar
  28. Kyriakou E, Chatzoglou E, Zouros E, Rodakis GC (2014a) The rRNA and tRNA transcripts of maternally and paternally inherited mitochondrial DNAs of Mytilus galloprovincialis suggest presence of a “degradosome” in mussel mitochondria and necessitate the re-annotation of the l-rRNA/CR boundary. Gene 540:78–85Google Scholar
  29. Kyriakou E, Chatzoglou E, Rodakis GC, Zouros E (2014b) Does the ORF in the control region of Mytilus mtDNA code for a protein product? Gene 546:448–450Google Scholar
  30. Kyriakou E, Kravariti L, Vasilopoulos T, Zouros E, Rodakis GC (2015) A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission. Gene 562:83–94Google Scholar
  31. Ladoukakis MD, Zouros E (2001) Direct evidence for homologous recombination in mussel (Mytilus galloprovincialis) mitochondrial DNA. Mol Biol Evol 18:1168–1175Google Scholar
  32. Ladoukakis M, 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 11:755–769Google Scholar
  33. Longo FJ, Dornfeld EJ (1967) The fine structure of differentiation of spermatid differentiation in the mussel, Mytilus edulis. J Ultrastruct Res 20:462–480Google Scholar
  34. Machordom A, Araujo R, Toledo C, Zouros E, Ladoukakis EM (2014) Female-dependent transmission of paternal mtDNA is a shared feature of bivalve species with doubly uniparental inheritance (DUI) of mitochondrial DNA. J Zoolog Syst Evol Res.  https://doi.org/10.1111/jzs.12096Google Scholar
  35. Obata M, Sano N, Kawamura K, Komaru A (2007) Inheritance of two M type mitochondrial DNA from sperm and unfertilized eggs to offspring in Mytilus galloprovincialis. Dev Growth Differ 49:335–344Google Scholar
  36. Obata M, Sano N, Komaru A (2011) Different transcriptional ratios of male and female transmitted mitochondrial DNA and tissue-specific expression patterns in the blue mussel, Mytilus galloprovincialis. Dev Growth Differ 53(7):878–886.  https://doi.org/10.1111/j.1440-169X.2011.01294.xCrossRefGoogle Scholar
  37. Passamonti M, Ghiselli F (2009) Doubly uniparental inheritance: two mitochondrial genomes, one precious model for organelle DNA inheritance and evolution. DNA Cell Biol 28:79–89Google Scholar
  38. Piganeau G, Gardner M, Eyre-Walker A (2004) A broad survey of recombination in animal mitochondria. Mol Biol Evol 21:2319–2325Google Scholar
  39. Sano N, Obata M, Komaru A (2007) Quantitation of the male and female types of mitochondrial DNA in a blue mussel, Mytilus galloprovincialis, using real-time polymerase chain reaction assay. Dev Growth Differ 49:67–72Google Scholar
  40. Sano N, Obata M, Komaru A (2010) Mitochondrial DNA transmitted from sperm in the blue mussel Mytilus galloprovincialis showing doubly uniparental inheritance of mitochondria, quantified by real-time PCR. Zoolog Sci 27:611–614Google Scholar
  41. Skibinski DOF, Gallagher C, Beynon CM (1994a) Mitochondrial DNA inheritance. Nature 368:817Google Scholar
  42. Skibinski DOF, Gallagher C, Beynon CM (1994b) Sex-limited mitochondrial DNA transmission in the marine mussel Mytilus edulis. Genetics 138:801–809Google Scholar
  43. Stewart DT, Kenchington ER, Singh RK, Zouros E (1996) Degree of selective constraint as an explanation of the differentrates of evolution of gender-specific mitochondrial DNA lineages in the mussel Mytilus. Genetics 143:1349–1357Google Scholar
  44. Sutovsky P, Moreno RD, Ramalho-Santos J et al (1999) Development – ubiquitin tag for sperm mitochondria. Nature 402:371–372Google Scholar
  45. Sutovsky P, Moreno RD, Ramalho-Santos J et al (2000) Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol Reprod 63:582–590Google Scholar
  46. Theologidis I (2007) The reversal of the transmission route of mitochondrial DNA in bivalves and its phylogenetic implications. PhD thesis, Department of Biology, University of CreteGoogle Scholar
  47. Theologidis I, Fodelianakis S, Gaspar MB, Zouros E (2008) Doubly uniparental inheritance (DUI) of mitochondrial DNA in Donax trunculus (Bivanvia: Donacidae) and the problem of its sporadic detection in Bivalvia. Evolution 62:959–970Google Scholar
  48. Tsaousis AD, Martin DP, Ladoukakis ED, Posada D, Zouros E (2005) Widespread recombination in published animal mtDNA sequences. Mol Biol Evol 22:925–933Google Scholar
  49. Venetis C, Theologidis I, Zouros E, Rodakis GC (2006) No evidence for presence of maternal mitochondrial DNA in the sperm of Mytilus galloprovincialis males. Proc R Soc B 273:2483–2489Google Scholar
  50. Venetis C, Theologidis I, Zouros E, Rodakis GC (2007) A mitochondrial genome with a reversed transmission route in the Mediterranean mussel Mytilus galloprovincialis. Gene 406:79–90Google Scholar
  51. Verdonk NH, van den Biggelaar AM (1983) Earrly development and the formation of the germ leyers. In: Verdonk NH, van den JAM B, Tompa AS (eds) The Mollusca, vol 3. Development. Acamedic Press, New York, pp 91–122Google Scholar
  52. White DJ, Wolff JN, Pierson M, Gemmell NJ (2008) Revealing the hidden complexities of mtDNA inheritance. Mol Ecol 17:4925–4942Google Scholar
  53. Zouros E (2000) The exceptional mitochondrial DNA system of the mussel family Mytilidae. Genes Genet Syst 75:313–318Google Scholar
  54. Zouros E (2013) Biparental inheritance through uniparental transmissions: the doubly uniparental Inheritance (DUI) of mitochondrial DNA. Evol Biol 40:1–31Google Scholar
  55. Zouros E, Freeman RK, Oberhauser Ball A, Pogson GH (1992a) Direct evidence of extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359:412–414Google Scholar
  56. Zouros E, Freeman RK, Oberhauser Ball A, Pogson GH (1992b) Direct evidence of extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359:412–414Google Scholar
  57. Zouros E, Oberhouser Ball A, Saavedra C, Freeman KR (1994a) Mitochondrial DNA inheritance. Nature 368:817Google Scholar
  58. Zouros E, Oberhauser Ball A, Saavedra C, Freeman KR (1994b) An unusul type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci U S A 91:7463–7467Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of BiologyUniversity of CreteHeraklionGreece
  2. 2.Department of BiologyNational and Kapodistrian University of AthensAthensGreece

Personalised recommendations