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

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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.

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References

  • Belliard G, Vadel F, Pelletier G (1979) Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature 281:401–403

    CAS  Google Scholar 

  • Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:11331–11338

    CAS  Google Scholar 

  • Birky CW Jr (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu Rev Genet 35:125–148

    CAS  PubMed  Google Scholar 

  • Borkhardt B, Olson LW (1983) Paternal inheritance of the mitochondrial DNA in interspecific crosses of the aquatic fungus Allomyces. Curr Genet 7:403–404

    CAS  Google Scholar 

  • Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43

    CAS  PubMed  Google Scholar 

  • Carr CM, Kim PS (1993) A spring-loaded mechanism for the conformational change of influenza hemagglutinin. Cell 73:823–832

    CAS  PubMed  Google Scholar 

  • Cermakian N, et al (1997) On the evolution of the single-subunit RNA polymerase. J Mol Evol 45:671–681

    CAS  PubMed  Google Scholar 

  • Chung KR, Leuchtmann A, Schardl CL (1996) Inheritance of mitochondrial DNA and plasmids in the ascomycetous fungus, Epichloe typhian. Genetics 142:259–265

    CAS  PubMed  Google Scholar 

  • 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 19:129–137

    CAS  PubMed  Google Scholar 

  • Crochet PA, Desmarais E (2000) Slow rate of evolution in the mitochondrial control region of gulls (Aves: Laridae). Mol Biol Evol 17:1797–1806

    CAS  PubMed  Google Scholar 

  • Dee J (1960) A mating-type system in an acellular slime-mould. Nature 185:780–781

    Google Scholar 

  • 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 211–251

  • Dee J (1987) Genes and development in Physarum. Trends Genet 3:208–213

    Article  Google Scholar 

  • Dujon B, Slonimski PP, Weill L (1974) Mitochondrial genetics IX: a model for recombination and segregation of mitochondrial genomes in Saccharomyces cerevisiae. Genetics 78:415–437

    CAS  PubMed  Google Scholar 

  • 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 218:419–422

    CAS  Google Scholar 

  • Eyre-Walker A, Smith NH, Smith JM (1999) How clonal are human mitochondria? Proc R Soc Lond B Biol Sci 266:477–483

    CAS  PubMed  Google Scholar 

  • Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715–6719

    CAS  PubMed  Google Scholar 

  • Griffiths AJF (1995) Natural plasmids of filamentous fungi. Microbiol Rev 59:673–685

    CAS  PubMed  Google Scholar 

  • Griffiths AJF, Bertrand H (1984) Unstable cytoplasm in Hawaiian strains of Neurospora intermedia. Curr Genet 8:387–398

    Google Scholar 

  • Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352:255–257

    Article  CAS  PubMed  Google Scholar 

  • 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 267:797–805

    Article  CAS  PubMed  Google Scholar 

  • Hutchinson CA, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538

    PubMed  Google Scholar 

  • 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 92:4542–4546

    CAS  PubMed  Google Scholar 

  • Kawano S, Kuroiwa T (1989) Transmission pattern of mitochondrial DNA during plasmodium formation in Physarum polycephalum. J Gen Microbiol 135:1559–1566

    Google Scholar 

  • Kawano S, Anderson RW, Nanba T, Kuroiwa T (1987) Polymorphisms and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J Gen Microbiol 133:3175–3182

    CAS  PubMed  Google Scholar 

  • Kawano S, Takano H, Mori K, Kuroiwa T (1991a) A mitochondrial plasmid that promotes mitochondrial fusion in Physarum polycephalum. Protoplasma 160:167–169

    Google Scholar 

  • Kawano S, Takano H, Mori K, Kuroiwa T (1991b) The oldest laboratory strain of Physarum polycephalum. Physarum Newsl 22:70–75

    Google Scholar 

  • Kawano S, Takano H, Imai J, Mori K, Kuroiwa T (1993) A genetic system controlling mitochondrial fusion in the slime mould, Physarum polycephalum. Genetics 133:213–224

    CAS  PubMed  Google Scholar 

  • Kawano S, Takano H, Kuroiwa T (1995) Sexuality of mitochondria: fusion, recombination, and plasmids. Int Rev Cytol 161:49–110

    CAS  PubMed  Google Scholar 

  • 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 73:126–131

    Google Scholar 

  • Kirouac-Brunet J, Mansson S, Pallota D (1981) Multiple allelism at the matB locus in Physarum polycephalum. Can J Genet Cytol 23:9–16

    Google Scholar 

  • Kondo R, Satta Y, Matsuura ET, Ishiwa H, Takahata N, Chigusa SI (1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126:657–663

    CAS  PubMed  Google Scholar 

  • Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298:481–483

    CAS  PubMed  Google Scholar 

  • Kvist L, Martens J, Nazarenko AA, Orell M (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Mol Biol Evol 20:243–247

    Article  CAS  PubMed  Google Scholar 

  • May G, Taylor JW (1989) Independent transfer of mitochondrial plasmids in Neurospora crassa. Nature 359:320–322

    Article  Google Scholar 

  • Meinhardt F, Kempken F, Kämper J, Esser K (1990) Linear plasmids among eukaryotes: fundamentals and application. Curr Genet 17:89–95

    CAS  PubMed  Google Scholar 

  • 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 19:55–60

    CAS  PubMed  Google Scholar 

  • 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 164:963–975

    CAS  PubMed  Google Scholar 

  • 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 7:934–940

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa CC, Jones EP, Miller DL (1998) Mitochondrial DNA rearrangements associated with mF plasmid integration and plasmodial longevity in Physarum polycephalum. Curr Genet 33:178–187

    Article  CAS  PubMed  Google Scholar 

  • 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 148:1907–1919

    PubMed  Google Scholar 

  • Nishibayashi S, Kawano S, Kuroiwa T (1987) Light and electron microscopic observation of mitochondrial fusion in plasmodia induced sporulation in Physarum polycephalum. Cytologica 52:599–614

    Google Scholar 

  • 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 111:105–117

    Article  Google Scholar 

  • 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 28:272–275

    Article  CAS  PubMed  Google Scholar 

  • 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 7:83–91

    CAS  PubMed  Google Scholar 

  • Sasaki N, Sakai A, Kawano S, Kuroiwa H, Kuroiwa T (1998) DNA synthesis in isolated mitochondrial nucleoids from plasmodia of Physarum polycephalum. Protoplasma 203:221–231

    CAS  Google Scholar 

  • 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 17:474–488

    CAS  PubMed  Google Scholar 

  • Schardl CL, Pring DR, Lonsdale DM (1985) Mitochondrial DNA rearrangements associated with fertile revertants of S-type male-sterile maize. Cell 43:361–368

    CAS  PubMed  Google Scholar 

  • Schwartz M, Vissing J (2002) Paternal inheritance of mitochondrial DNA. N Engl J Med 347:576–580

    Article  PubMed  Google Scholar 

  • Solignac M, Monnerot M, Mounolou JC (1983) Mitochondrial DNA heteroplasmy in Drosophila mauritiana. Proc Natl Acad Sci USA 80:6942–6946

    CAS  PubMed  Google Scholar 

  • Takano H, Kawano S, Kuroiwa T (1992) Constitutive homologous recombination between mitochondrial DNA and a linear mitochondrial plasmid in Physarum polycephalum. Curr Genet 22:221–227

    CAS  PubMed  Google Scholar 

  • 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 29:257–264

    CAS  PubMed  Google Scholar 

  • Takano H, Kuroiwa T, Kawano S (1997) Mitochondrial fusion promoting plasmid. Cell Struct Funct 22:299–308

    CAS  PubMed  Google Scholar 

  • 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 115:255–261

    Article  CAS  PubMed  Google Scholar 

  • Vogt VM, Braun R (1977) The replication of ribosomal DNA in Physarum polycephalum. Eur J Biochem 80:557–566

    CAS  PubMed  Google Scholar 

  • Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772

    CAS  PubMed  Google Scholar 

  • Wilkinson GS, Chapman AM (1991) Length and sequence variation in evening bat D-loop mtDNA. Genetics 128:607–617

    CAS  PubMed  Google Scholar 

  • Yang X, Griffiths AJF (1993a) Male transmission of linear plasmids and mitochondrial DNA in the fungus Neurospora. Genetics 134:1055–1062

    CAS  PubMed  Google Scholar 

  • Yang X, Griffiths AJF (1993b) Plasmid suppressors active in the sexual cycle of Neurospora intermedia. Genetics 135:993–1002

    CAS  PubMed  Google Scholar 

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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.

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  1. Laboratory of Plant Life System, Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Bldg. FSB-601, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8562, Japan

    Rakusa Sakurai, Hideo Nomura, Yohsuke Moriyam & Shigeyuki Kawano

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  1. Rakusa Sakurai
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  2. Hideo Nomura
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  3. Yohsuke Moriyam
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  4. Shigeyuki Kawano
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Correspondence to Shigeyuki Kawano.

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Communicated by M. Brunner

The first two authors have equally contributed to this work

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Sakurai, R., Nomura, H., Moriyam, Y. et al. The mitochondrial plasmid of the true slime mold Physarum polycephalum bypasses uniparental inheritance by promoting mitochondrial fusion. Curr Genet 46, 103–114 (2004). https://doi.org/10.1007/s00294-004-0512-x

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