Journal of Plant Research

, Volume 123, Issue 2, pp 139–148 | Cite as

Maternal inheritance of mitochondria: multipolarity, multiallelism and hierarchical transmission of mitochondrial DNA in the true slime mold Physarum polycephalum

  • Yohsuke MoriyamaEmail author
  • Shigeyuki KawanoEmail author
JPR Symposium Cytoplasmic inheritance


Direct evidence of digestion of paternal mitochondrial DNA (mtDNA) has been found in the true slime mold Physarum polycephalum. This is the first report on the selective digestion of mtDNA inside the zygote, and is striking evidence for the mechanism of maternal inheritance of mitochondria. Moreover, two mitochondrial nuclease activities were detected in this organism as candidates for the nucleases responsible for selective digestion of mtDNA. In the true slime mold, there is an additional feature of the uniparental inheritance of mitochondria. Although mitochondria are believed to be inherited from the maternal lineage in nearly all eukaryotes, the mating types of the true slime mold P. polycephalum is not restricted to two: there are three mating loci—matA, matB, and matC—and these loci have 16, 15, and 3 alleles, respectively. Interestingly, the transmission patterns of mtDNA are determined by the matA locus, in a hierarchical fashion (matA hierarchy) as follows: matA7 > matA2 > matA11 > matA12 > matA15/matA16 > matA1 > matA6. The strain possessing the higher status of matA would be the mtDNA donor in crosses. Furthermore, we have found that some crosses showed biparental inheritance of mitochondria. This review describes the phenomenon of hierarchical transmission of mtDNA in true slime molds, and discusses the presumed molecular mechanism of maternal and biparental inheritance.


Didymium iridis Hierarchical transmission Selective digestion Maternal inheritance of mitochondria mtDNA Physarum polycephalum 



The authors thank Dr. Tsuneyoshi Kuroiwa for his thoughtful suggestions, generous support and encouragement. We also would like to thank Dr. J. Mark Cock for checking our manuscript. This study was supported by grants for Scientific Research in Priority Areas (no. 13440246, no. 15440246, and 20440123 to S.K.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.


  1. Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci USA 93:13859–13863CrossRefPubMedGoogle Scholar
  2. Aoyama H, Hagiwara Y, Misumi O, Kuroiwa T, Nakamura S (2006) Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 228:231–241CrossRefPubMedGoogle Scholar
  3. Bailey J, Anderson RW, Dee J (1990) Cellular events during sexual development from amoeba to plasmodium in the slime mould Physarum polycephalum. J Gen Microbiol 136:739–751PubMedGoogle Scholar
  4. Baldauf SL (2003) The deep roots of eukaryotes. Science 300:1703–1706CrossRefPubMedGoogle Scholar
  5. Barr CM, Neiman M, Taylor DR (2005) Inheritance and recombination of mitochondrial genomes in plants, fungi and animals. New Phytol 168:39–50CrossRefPubMedGoogle Scholar
  6. Baur E (1909) Das Wesen und die Erblichkeitsverhaltniss der “varietates albomarginatae hort” von Pelargonium zonale. Z Vererbungsl 1:330–351Google Scholar
  7. Birky CW (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci USA 92:1331–11338CrossRefGoogle Scholar
  8. Birky CW (2001) The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms and models. Annu Rev Genet 35:125–148CrossRefPubMedGoogle Scholar
  9. Casselton LA (2008) Fungal sex genes-searching for the ancestors. Bioessays 30:711–714CrossRefPubMedGoogle Scholar
  10. Correns C (1909) Verebungsversuche mit blass (gelb) grunen und buntblattrigen sippen bei Mirabilis jalapa, Urica pilulifera und Lunaria annura. Z Verebungsl 1:291–329CrossRefGoogle Scholar
  11. Corriveau JL, Coleman AW (1991) Monitoring by epifluorescence microscopy of organelle DNA fate during pollen development in five angiosperm species. Dev Biol 147:271–280CrossRefPubMedGoogle Scholar
  12. Creasey AM, Ranford-Cartwright LC, Moore DJ, Williamson DH, Wilson RJ, Walliker D, Carter R (1993) Uniparental inheritance of the mitochondrial gene cytochrome b in Plasmodium falciparum. Curr Genet 23:360–364CrossRefPubMedGoogle Scholar
  13. Dawid IB, Blackler AW (1972) Maternal and cytoplasmic inheritance of mitochondrial DNA in Xenopus. Dev Biol 29:152–162CrossRefPubMedGoogle Scholar
  14. Dee J (1966) Multiple alleles and other factors affecting plasmodium formation in the true slime mould Physarum polycephalum Schw. J Protozool 13:610–616Google Scholar
  15. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715–6719CrossRefPubMedGoogle Scholar
  16. Hayashi J, Yonekawa H, Gotoh O, Motohashi J, Tagashira Y (1978) Two different molecular types of rat mitochondrial DNAs. Biochem Biophys Res Commun 81:871–877CrossRefPubMedGoogle Scholar
  17. Holt CE, Huttermann A, Heunert HH, Galle HK (1980) Role of mating specificity genes in Physarum polycephalum. Eur J Cell Biol 22:316Google Scholar
  18. Hutchison CA III, Newbold JE, Potter SS, Edgell MH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538CrossRefPubMedGoogle Scholar
  19. Iwanaga A, Sasaki A (2004) Evolution of hierarchical cytoplasmic inheritance in the plasmodial slime mold Physarum polycephalum. Evolution 58:710–722PubMedGoogle Scholar
  20. Kaneda H, Hayashi J, Takahama S, Taya C, Lindahl KF et al (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad Sci USA 92:4542–4546CrossRefPubMedGoogle Scholar
  21. Kawano S, Kuroiwa T (1989) Transmission pattern of mitochondrial DNA during plasmodium formation in Physarum polycephalum. J Gen Microbiol 135:1559–1566Google Scholar
  22. Kawano S, Anderson RW, Nanba T, Kuroiwa T (1987a) Polymorphism and uniparental inheritance of mitochondrial DNA in Physarum polycephalum. J Gen Microbiol 133:3175–3182PubMedGoogle Scholar
  23. Kawano S, Kuroiwa T, Anderson RW (1987b) A third multiallelic mating-type locus in Physarum polycephalum. J Gen Microbiol 133:2539–2546Google Scholar
  24. Kawano S, Takano H, Kuroiwa T (1995) Sexuality of mitochondria: fusion, recombination, and plasmids. Int Rev Cytol 161:49–110CrossRefPubMedGoogle Scholar
  25. 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
  26. Kroon AM, de Vos WM, Bakker H (1978) The heterogeneity of rat-liver mitochondrial DNA. Biochim Biophys Acta 519:269–273PubMedGoogle Scholar
  27. Kuroiwa T (1985) Mechanisms of maternal inheritance of chloroplast DNA: an active digestion hypothesis. Microbiol Sci 2:267–270PubMedGoogle Scholar
  28. Kuroiwa T (1991) The replication, differentiation, and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62CrossRefGoogle Scholar
  29. Kuroiwa T, Kawano S, Nishibayashi S, Sato C (1982) Epifluorescent microscopic evidence for maternal inheritance of chloroplast DNA. Nature 298:481–483CrossRefPubMedGoogle Scholar
  30. May G, Matzke E (1995) Recombination and variation at the A mating-type of Coprinus cinereus. Mol Biol Evol 12:794–802Google Scholar
  31. Meland S, Johansen S, Johansen T, Haugli K, Haugli F (1991) Rapid disappearance of one parental mitochondrial genotype after isogamous mating in the myxomycete Physarum polycephalum. Curr Genet 19:55–59CrossRefPubMedGoogle Scholar
  32. Mirfakhrai M, Tanaka Y, Yanagisawa K (1990) Evidence for mitochondrial DNA polymorphism and uniparental inheritance in the cellular slime mold Polysphondylium pallidum: effect of intraspecies mating on mitochondrial DNA transmission. Genetics 24:607–613Google Scholar
  33. 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
  34. Moriyama Y, Yamazaki T, Nomura H, Sasaki N, Kawano S (2005) Early zygote-specific nuclease in mitochondria of the true slime mold Physarum polycephalum. Curr Genet 48:334–343CrossRefPubMedGoogle Scholar
  35. Moriyama Y, Itoh K, Nomura H, Kawano S (2009) Disappearance of mtDNA during mating of the true slime mold Didymium iridis. Cytologia 74:159–164CrossRefGoogle Scholar
  36. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (1999) The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65CrossRefPubMedGoogle Scholar
  37. Pallotta DJ, Youngman PJ, Shinnick TM, Holt CE (1979) Kinetics of mating in Physarum polycephalum. Mycologia 71:68–84CrossRefPubMedGoogle Scholar
  38. Reilly JG, Thomas CA Jr (1980) Length polymorphisms, restriction site variation, and maternal inheritance of mitochondrial DNA of Drosophila melanogaster. Plasmid 3:109–115CrossRefPubMedGoogle Scholar
  39. Shinnick TM, Pallotta DJ, Jones-Brown YVR, Youngman PJ, Holt CE (1978) A gene imz affecting the pH sensitivity of zygote formation in Physarum polycephalum. Curr Microbiol 1:163–166CrossRefGoogle Scholar
  40. Silliker ME, Collins OR (1988) Non-mendelian inheritance of mitochondrial DNA and ribosomal DNA in the myxomycete, Didymium iridis. Mol Gen Genet 213:370–378CrossRefPubMedGoogle Scholar
  41. Silliker ME, Liles JL, Monroe JA (2002) Patterns of mitochondrial inheritance in the myxogastrid Didymium iridis. Mycologia 94:939–946CrossRefGoogle Scholar
  42. Specht CA, Novotny CP, Ullrich RC (1992) Mitochondrial DNA of Schizophyllum commune: restriction map, genetic map, and mode of inheritance. Curr Genet 22:129–134CrossRefPubMedGoogle Scholar
  43. Takano H, Abe T, Sakurai R, Moriyama Y, Miyazawa Y, Nozaki H, Kawano S, Sasaki N, Kuroiwa T (2001) The complete DNA sequence of the mitochondrial genome of Physarum polycephalum. Mol Gen Genet 264:539–545CrossRefPubMedGoogle Scholar
  44. Wilch G, Ward S, Castle A (1992) Transmission of mitochondrial DNA in Ustilago violacea. Curr Genet 22:135–140CrossRefPubMedGoogle Scholar
  45. Youngman PJ, Pallotta DJ, Hosler B, Struhl G, Holt CE (1979) A new mating compatibility locus in Physarum polycephalum. Genetics 91:683–693PubMedGoogle Scholar
  46. Youngman PJ, Anderson RW, Holt CE (1981) Two multiallelic mating compatibility loci separately regulate zygote formation and zygote differentiation in the myxomycete Physarum polycephalum. Genetics 97:513–530PubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2010

Authors and Affiliations

  1. 1.Department of Integrated Biosciences, Graduate School of Frontier SciencesUniversity of TokyoKashiwaJapan

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