Abstract
Although mitochondrial DNA (mtDNA) is transmitted to progeny from one parent only in Physarum polycephalum, the mtDNAs of progeny of mF+ plasmodia vary in structure. To clarify the mechanisms associated with the mitochondrial plasmid mF that generate mtDNA polymorphisms, 91 progeny of four strains (KM88 × JE8, KM88 × TU111, KM88 × NG111, Je90) were investigated using RFLP analysis, PCR, and pulse-field gel electrophoresis (PFGE). Nine mtDNA rearrangement types were found, with rearrangements occurring exclusively in the mF regions. PFGE revealed that, in the groups containing rearranged mtDNA, the linear mF–mtDNA recombinants had recircularized. Sequencing the rearranged region of one of the progeny suggested that the mF plasmid and the mtDNA recombine primarily at the ID sequences, linearizing the circular mtDNA. Recombination between the terminal region of the mF plasmid and a region about 1 kbp upstream of the mitochondrial/plasmid ID sequence results in a rearranged circular mtDNA, with variations caused by differences in the secondary recombination region.
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References
Albert B, Godelle B, Gouyon P (1998) Evolution of the plant mitochondrial genome: dynamics of duplication and deletion of sequences. J Mol Evol 46:155–158
Cermakian N, Ikeda TM, Miramontes P, Lang BF, Gray MW, Cedergren R (1997) On the evolution of single-subunit RNA polymerases. J Mol Evol 45:671–681
Fauron C, Casper M, Gao Y, Moore B (1995) The maize mitochondrial genome: dynamic, yet functional. Trends Genet 11:228–235
Griffiths AJF (1992) Fungal senescence. Annu Rev Genet 26:351–372
Griffiths AJF (1995) Natural plasmid of filamentous fungi. Microbiol Rev 59:673–685
Janska H, Woloszynska M (1997) The dynamic nature of plant mitochondrial genome organization. Acta Biochim Pol 44:239–250
Kawano S, Kuroiwa T (1989) Transmission pattern of mitochondrial DNA during plasmodium formation in Physarum polycephalum. J Gen Microbiol 135:1559–1566
Kawano S, Takano H, Kuroiwa T (1995) Sexuality of mitochondria: fusion, recombination, and plasmids. Int Rev Cytol 161:49–110
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
Kawano S, Takano H, Mori K, Kuroiwa T (1991a) A mitochondrial plasmid that promotes mitochondrial fusion in Physarum polycephalum. Protoplasma 160:167–169
Kawano S, Takano H, Mori K, Kuroiwa T (1991b) The oldest laboratory strain of Physarum polycephalum. Physarum Newsl 22:70–75
Kirouac-Brunet J, Mansson S, Pallota D (1981) Multiple allelism at the matB locus in Physarum polycephalum. Can J Genet Cytol 23: 9–16
Meinhardt F, Kempken F, Kämper J, Esser K (1990) Linear plasmids among eukaryotes: fundamentals and application. Curr Genet 17:89–97
Moeykens CA, Mackenzie SA, Shoemaker RC (1995) Mitochondrial genome diversity in soybean: repeats and rearrangements. Plant Mol Biol 29:245–254
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
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
Ohta T, Kawano S, Kuroiwa T (1993) Restriction of amoebo-flagellate (AF) transformation to interphase is related to M phase replication of the centrosome complex in the amoebae of the true slime mould, Physarum polycephalum: a three-dimensional approach. J Struct Biol 111:105–117
Ryan R, Grant D, Chang KS, Swift H (1978) Isolation and characterization of mitochondrial DNA from Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 75:3268–3272
Sakurai R, Sasaki N, Takano H, Abe T, Kawano S (2000) In vivo conformation of mitochondrial DNA revealed by pulse-field gel electrophoresis in the true slime mold, Physarum polycephalum. DNA Res 7:83–91
Sakurai R, Nomura H, Moriyama Y, Kawano S (2004) The mitochondrial plasmid of the true slime mold Physarum polycephalum bypasses uniparental inheritance by promoting mitochondrial fusion. Curr Genet 46:103–114
Sambrook J, Frich EH, Manistis T (1989) Transfer of DNA to nitrocellulose filters. In: Ford N, Nolan C, Ferguson M (eds) Molecular cloning: laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp 9.38–9.40
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
Schardl CL, Lonsdale DM, Pring DR, Rose KR (1984) Linearization of maize mitochondrial chromosomes by recombination with linear episomes. Nature 310:292–296
Schardl CL, Pring DR, Lonsdale DM (1985) Mitochondrial DNA rearrangements associated with fertile revertants of S-type male-sterile maize. Cell 43:361–368
Takano H (2001) Intimate relationship between mtDNA, plasmids, and the fusion of mitochondria. J Plant Res 113:223–229
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
Takano H, Kawano S, Kuroiwa T (1994) Genetic organization of a linear mitochondrial plasmid (mF) that promotes mitochondrial fusion in Physarum polycephalum. Curr Genet 26:506–511
Takano H, Kawano S, Suyama Y, Kuroiwa T (1990) Restriction map of the mitochondrial DNA of the true slime mould, Physarum polycephalum: linear form and long tandem duplication. Curr Genet 18:125–131
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
Takano H, Abe T, Sakurai R, Moriyama Y, Miyazawa Y, et al (2001) The complete DNA sequence of the mitochondrial genome of Physarum polycephalum. Mol Gen Genet 264:539–545
Turner G, Earl AJ, Greaves DR (1982) Interspecies variation and recombination of mitochondrial DNA in the Aspergillus nidulans species group and the selection of species-specific sequences by nuclear background. In: Slonimski P, Borst P, Attardi G (eds) Mitochondrial genes. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp 411–414
Ward BL, Anderson RS, Bendich AJ (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25:793–803
Yang X, Griffiths AJF (1993) Plasmid suppressors active in the sexual cycle of Neurospora intermedia. Genetics 135:993–1002
Acknowledgements
We would like to thank Prof. T. Kuroiwa (Department of Life Science, College of Science, Rikkyo University) for helpful discussions 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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Nomura, H., Moriyama, Y. & Kawano, S. Rearrangements in the Physarum polycephalum mitochondrial genome associated with a transition from linear mF-mtDNA recombinants to circular molecules. Curr Genet 47, 100–110 (2005). https://doi.org/10.1007/s00294-004-0540-6
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DOI: https://doi.org/10.1007/s00294-004-0540-6