Current Genetics

, Volume 46, Issue 2, pp 103–114 | Cite as

The mitochondrial plasmid of the true slime mold Physarum polycephalum bypasses uniparental inheritance by promoting mitochondrial fusion

  • Rakusa Sakurai
  • Hideo Nomura
  • Yohsuke Moriyam
  • Shigeyuki Kawano
Research Article

Abstract

Mitochondrial DNA (mtDNA) is inherited maternally in most eukaryotes. Linear mitochondrial plasmids in higher plants and fungi are also transmitted from the maternal parent to the progeny. However, mF, which is a mitochondrial linear plasmid of Physarum polycephalum, evades uniparental mitochondrial inheritance. We examined 36 myxamoebal strains of Physarum and isolated three novel mF+ strains (JE8, TU111, NG111) that harbored free mF plasmids. These strains were mated with the mF strain KM88. Of the three mF × mF+ crosses, only KM88 × JE8 displayed complete uniparental inheritance. However, in KM88 × TU111 and KM88 × NG111, the mtDNA of KM88 and mF of TU111 and NG111 were inherited by the plasmodia and showed recombination. For example, although the mtDNA of TU111 was eliminated, the mF of TU111 persisted and became inserted into the mtDNA of KM88, such that recombinant mtDNA represented 80% of the total mtDNA. The parental mitochondria fused to yield giant mitochondria with two or more mitochondrial nucleoids. The mF appears to exchange mitochondria from the recipient (paternal) to the donor (maternal) by promoting mitochondrial fusion.

Keywords

Mitochondria Fusion Plasmid Uniparental inheritance Physarum polycephalum 

Notes

Acknowledgements

We would like to thank Prof. T. Kuroiwa (Department of Life Science, College of Science, Rikkyo University) for helpful discussion and Dr. H. Takano (Department of Biological Science, Faculty of Science, Kumamoto University) for helpful technical advice. This study was supported by grants to S.K. for Scientific Research in Priority Areas (nos. 13440246, 15370027) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

References

  1. Belliard G, Vadel F, Pelletier G (1979) Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 281:401–403Google Scholar
  2. Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338Google Scholar
  3. Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148PubMedGoogle Scholar
  4. Borkhardt B, Olson LW (1983) Paternal inheritance of the mitochondrial DNA in interspecific crosses of the aquatic fungus Allomyces. Curr Genet 7:403–404Google Scholar
  5. Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43PubMedGoogle Scholar
  6. Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823–832PubMedGoogle Scholar
  7. Cermakian N, et al (1997) On the evolution of the single-subunit RNA polymerase. J Mol Evol 45:671–681PubMedGoogle Scholar
  8. Chung KR, Leuchtmann A, Schardl CL (1996) Inheritance of mitochondrial DNA and plasmids in the ascomycetous fungus, Epichloe typhian. Genetics 142:259–265PubMedGoogle Scholar
  9. Court DA, Griffiths AJF, Kraus SR, Russell PJ, Bertrand H (1991) A new senescence-inducing mitochondrial linear plasmid in field-isolated Neurospora crassa strains from India. Curr Genet 19:129–137PubMedGoogle Scholar
  10. Crochet PA, Desmarais E (2000) Slow rate of evolution in the mitochondrial control region of gulls (Aves: Laridae). Mol Biol Evol 17:1797–1806PubMedGoogle Scholar
  11. Dee J (1960) A mating-type system in an acellular slime-mould. Nature 185:780–781Google Scholar
  12. Dee J (1982) Genetics of Physarum polycephalum. In: Aldrich HC, Daniel JW (eds) Cell biology of Physarum and Didymium, vol 1. Academic, New York, pp 211–251Google Scholar
  13. Dee J (1987) Genes and development in Physarum. Trends Genet 3:208–213CrossRefGoogle Scholar
  14. Dujon B, Slonimski PP, Weill L (1974) Mitochondrial genetics IX: a model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78:415–437PubMedGoogle Scholar
  15. Erickson L, Kemble R, Swanson E (1989) The Brassica mitochondrial plasmid can be sexually transmitted. Pollen transfer of a cytoplasmic genetic element. Mol Gen Genet 218:419–422Google Scholar
  16. Eyre-Walker A, Smith NH, Smith JM (1999) How clonal are human mitochondria? Proc R Soc Lond B Biol Sci 266:477–483PubMedGoogle Scholar
  17. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715–6719PubMedGoogle Scholar
  18. Griffiths AJF (1995) Natural plasmids of filamentous fungi. Microbiol Rev 59:673–685PubMedGoogle Scholar
  19. Griffiths AJF, Bertrand H (1984) Unstable cytoplasm in Hawaiian strains of Neurospora intermedia. Curr Genet 8:387–398Google Scholar
  20. Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352:255–257CrossRefPubMedGoogle Scholar
  21. Handa H, Itani K, Sato H (2002) Structural features and expression analysis of a linear mitochondrial plasmid in rapeseed (Brassica napus L.). Mol Genet Genomics 267:797–805CrossRefPubMedGoogle Scholar
  22. Hutchinson CA, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538PubMedGoogle Scholar
  23. Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF, Yonekawa H (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542–4546PubMedGoogle Scholar
  24. Kawano S, Kuroiwa T (1989) Transmission pattern of mitochondrial DNA during plasmodium formation in Physarum polycephalum. J Gen Microbiol 135:1559–1566Google Scholar
  25. Kawano S, Anderson RW, Nanba T, Kuroiwa T (1987) Polymorphisms and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J Gen Microbiol 133:3175–3182PubMedGoogle Scholar
  26. Kawano S, Takano H, Mori K, Kuroiwa T (1991a) A mitochondrial plasmid that promotes mitochondrial fusion in Physarum polycephalum. Protoplasma 160:167–169Google Scholar
  27. Kawano S, Takano H, Mori K, Kuroiwa T (1991b) The oldest laboratory strain of Physarum polycephalum. Physarum Newsl 22:70–75Google Scholar
  28. Kawano S, Takano H, Imai J, Mori K, Kuroiwa T (1993) A genetic system controlling mitochondrial fusion in the slime mould, Physarum polycephalum. Genetics 133:213–224PubMedGoogle Scholar
  29. Kawano S, Takano H, Kuroiwa T (1995) Sexuality of mitochondria: fusion, recombination, and plasmids. Int Rev Cytol 161:49–110PubMedGoogle Scholar
  30. Kawano S, Abe T, Mori K, Takano H (1997) The origin of a linear mitochondrial plasmid (mF) that promotes mitochondrial fusion in laboratory strains of Physarum polycephalum. Proc Jpn Acad 73:126–131Google Scholar
  31. Kirouac-Brunet J, Mansson S, Pallota D (1981) Multiple allelism at the matB locus in Physarum polycephalum. Can J Genet Cytol 23:9–16Google Scholar
  32. Kondo R, Satta Y, Matsuura ET, Ishiwa H, Takahata N, Chigusa SI (1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126:657–663PubMedGoogle Scholar
  33. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298:481–483PubMedGoogle Scholar
  34. 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
  35. May G, Taylor JW (1989) Independent transfer of mitochondrial plasmids in Neurospora crassa. Nature 359:320–322CrossRefGoogle Scholar
  36. Meinhardt F, Kempken F, Kämper J, Esser K (1990) Linear plasmids among eukaryotes: fundamentals and application. Curr Genet 17:89–95PubMedGoogle Scholar
  37. Meland S, Johansen S, Johansen T, Haugli K, Haugli FS (1991) Rapid disappearance of one parental mitochondrial genotype after isogamous mating in the myxomycete Physarum polycephalum. Curr Genet 19:55–60PubMedGoogle Scholar
  38. Moriyama Y, Kawano S (2003) Rapid, selective digestion of mitochondrial DNA in accordance with the matA hierarchy of multiallelic mating types in the mitochondrial inheritance of Physarum polycephalum. Genetics 164:963–975PubMedGoogle Scholar
  39. Nakada K, Inoue K, Ono T, Sobe K, Ogura A, Goto YI, Nonaka I, Hayashi JI (2001) Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat Med 7:934–940CrossRefPubMedGoogle Scholar
  40. Nakagawa CC, Jones EP, Miller DL (1998) Mitochondrial DNA rearrangements associated with mF plasmid integration and plasmodial longevity in Physarum polycephalum. Curr Genet 33:178–187CrossRefPubMedGoogle Scholar
  41. Nesbø CL, Arab MO, Jakobsen KS (1998) Heteroplasmy, length and sequence variation in the control regions of three percid fish species (Perca fluviatilis, Acerina cernua, Stizostedion lucioperca). Genetics 148:1907–1919PubMedGoogle Scholar
  42. Nishibayashi S, Kawano S, Kuroiwa T (1987) Light and electron microscopic observation of mitochondrial fusion in plasmodia induced sporulation in Physarum polycephalum. Cytologica 52:599–614Google Scholar
  43. Ohta T, Kawano S, Kuroiwa T (1993) Restriction of amoebo-flagellate (AF) transformation to interphase is related to M phase replication of the centroseme complex in the amoebae of the true slime mould, Physarum polycephalum: a three-dimensional approach. J Struct Biol 111:105–117CrossRefGoogle Scholar
  44. Ono T, Isobe K, Nakada K, Hayashi JI (2001) Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat Genet 28:272–275CrossRefPubMedGoogle Scholar
  45. Sakurai R, Sasaki N, Takano H, Abe T, Kawano S (2000) In vivo conformation of mitochondrial DNA revealed by pulsed-field gel electrophoresis in the true slime mold, Physarum polycephalum. DNA Res 7:83–91PubMedGoogle Scholar
  46. Sasaki N, Sakai A, Kawano S, Kuroiwa H, Kuroiwa T (1998) DNA synthesis in isolated mitochondrial nucleoids from plasmodia of Physarum polycephalum. Protoplasma 203:221–231Google Scholar
  47. Savolainen P, Arvestad L, Lundeberg J (2000) mtDNA tandem repeats in dogs and wolves: mutation mechanism studied by analysis of the sequence of imperfect repeats. Mol Biol Evol 17:474–488PubMedGoogle Scholar
  48. Schardl CL, Pring DR, Lonsdale DM (1985) Mitochondrial DNA rearrangements associated with fertile revertants of S-type male-sterile maize. Cell 43:361–368PubMedGoogle Scholar
  49. Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576–580CrossRefPubMedGoogle Scholar
  50. Solignac M, Monnerot M, Mounolou JC (1983) Mitochondrial DNA heteroplasmy in Drosophila mauritiana. Proc Natl Acad Sci USA 80:6942–6946PubMedGoogle Scholar
  51. Takano H, Kawano S, Kuroiwa T (1992) Constitutive homologous recombination between mitochondrial DNA and a linear mitochondrial plasmid in Physarum polycephalum. Curr Genet 22:221–227PubMedGoogle Scholar
  52. Takano H, Mori K, Kawano S, Kuroiwa T (1996) Rearrangements of mitochondrial DNA and the mitochondrial fusion-promoting plasmid (mF) are associated with defective mitochondrial fusion in Physarum polycephalum. Curr Genet 29:257–264PubMedGoogle Scholar
  53. Takano H, Kuroiwa T, Kawano S (1997) Mitochondrial fusion promoting plasmid. Cell Struct Funct 22:299–308PubMedGoogle Scholar
  54. Takano H, Kawano S, Sasaki N, Kuroiwa H, Kuroiwa T (2002) Characterization of a putitive fusogen encoded in a mitochondrial plasmid of Physarum polycephalum. J Plant Res 115:255–261CrossRefPubMedGoogle Scholar
  55. Vogt VM, Braun R (1977) The replication of ribosomal DNA in Physarum polycephalum. Eur J Biochem 80:557–566PubMedGoogle Scholar
  56. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772PubMedGoogle Scholar
  57. Wilkinson GS, Chapman AM (1991) Length and sequence variation in evening bat D-loop mtDNA. Genetics 128:607–617PubMedGoogle Scholar
  58. Yang X, Griffiths AJF (1993a) Male transmission of linear plasmids and mitochondrial DNA in the fungus Neurospora. Genetics 134:1055–1062PubMedGoogle Scholar
  59. Yang X, Griffiths AJF (1993b) Plasmid suppressors active in the sexual cycle of Neurospora intermedia. Genetics 135:993–1002PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Rakusa Sakurai
    • 1
  • Hideo Nomura
    • 1
  • Yohsuke Moriyam
    • 1
  • Shigeyuki Kawano
    • 1
  1. 1.Laboratory of Plant Life System, Department of Integrated Biosciences, Graduate School of Frontier SciencesUniversity of TokyoChibaJapan

Personalised recommendations