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Paternal inheritance of mitochondria in Chlamydomonas

  • JPR Symposium
  • Cytoplasmic inheritance
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Abstract

To analyze mitochondrial DNA (mtDNA) inheritance, differences in mtDNA between Chlamydomonas reinhardtii and Chlamydomonas smithii, respiration deficiency and antibiotic resistance were used to distinguish mtDNA origins. The analyses indicated paternal inheritance. However, these experiments raised questions regarding whether paternal inheritance occurred normally. Mitochondrial nucleoids were observed in living zygotes from mating until 3 days after mating and then until progeny formation. However, selective disappearance of nucleoids was not observed. Subsequently, experimental serial backcrosses between the two strains demonstrated strict paternal inheritance. The fate of mt+ and mt− mtDNA was followed using the differences in mtDNA between the two strains. The slow elimination of mt+ mtDNA through zygote maturation in darkness was observed, and later the disappearance of mt+ mtDNA was observed at the beginning of meiosis. To explain the different fates of mtDNA, methylation status was investigated; however, no methylation was detected. Variously constructed diploid cells showed biparental inheritance. Thus, when the mating process occurs normally, paternal inheritance occurs. Mutations disrupting mtDNA inheritance have not yet been isolated. Mutations that disrupt maternal inheritance of chloroplast DNA (cpDNA) do not disrupt inheritance of mtDNA. The genes responsible for mtDNA inheritance are different from those of chloroplasts.

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References

  • 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 228:231–242

    Article  CAS  PubMed  Google Scholar 

  • Baur E (1909) Das wesen und die erblichkeitsverhaltnisse der “Varietates albo-marginatae hort” von Pelargonium zonale. Z Vererbungsl 1:330–351

    Google Scholar 

  • Beckers MC, Munaut C, Minet A, Matagne RF (1991) The fate of mitochondrial DNAs of mt+ and mt− origin in gametes and zygotes of Chlamydomonas. Curr Genet 20:239–243

    Article  CAS  PubMed  Google Scholar 

  • Bennoun P, Delosme M, Kuckt U (1991) Mitochondrial genetics of Chlamydomonas reinhardtii: resistance mutations marking the cytochrome b gene. Genetics 127:335–343

    CAS  PubMed  Google Scholar 

  • Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW (1987) Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci USA 84:2391–2395

    Article  CAS  PubMed  Google Scholar 

  • Burton WG, Grabowy CT, Sager R (1979) Role of methylation in the modification and restriction of chloroplast DNA in Chlamydomonas. Proc Natl Acad Sci USA 76:1390–1394

    Article  CAS  PubMed  Google Scholar 

  • Colin M, Dorthu MP, Duby F, Remacle C, Dinant M, Wolwertz MR, Duyckaerts C, Sluse F, Matagne RF (1995) Mutations affecting the mitochondrial genes encoding the cytochrome oxidase subunit I and apocytochrome b of Chlamydomonas reinhardtii. Mol Gen Genet 249:179–184

    Article  CAS  PubMed  Google Scholar 

  • Dorthu MP, Remy S, Michel-Wolwertz MR, Colleaux L, Breyer D, Beckers MC, Englebert S, Duyckaerts C, Sluse FE, Matagne RF (1992) Biochemical, genetic and molecular characterization of new respiratory-deficient mutants in Chlamydomonas reinhardtii. Plant Mol Biol 18:759–772

    Article  CAS  PubMed  Google Scholar 

  • Feng TY, Chiang KS (1984) The persistence of maternal inheritance in Chlamydomonas despite hypomethylation of chloroplast DNA induced by inhibitors. Proc Natl Acad Sci USA 81:3438–3442

    Article  CAS  PubMed  Google Scholar 

  • Galloway RE, Goodenough UW (1985) Genetic analysis of mating locus linked mutations in Chlamydomonas reinhardii. Genetics 111:447–461

    CAS  PubMed  Google Scholar 

  • Gillham NW (1994) Organelle genes and genomes. Oxford University Press, New York

    Google Scholar 

  • Gillham NW, Boynton JE, Johnson AM, Burkhart BD (1987) Mating type linked mutations which disrupt the uniparental transmission of chloroplast genes in Chlamydomonas. Genetics 115:677–684

    CAS  PubMed  Google Scholar 

  • Goodenough UW, Ferris PJ (1987) Genetic regulation of development in Chlamydomonas. In: Loomis WF (ed) Genetic regulation of development. Liss, New York, pp 171–189

    Google Scholar 

  • Grant D, Chiang KS (1980) Physical mapping and characterization of Chlamydomonas mitochondrial DNA molecules: their unique ends, sequence homogeneity, and conservation. Plasmid 4:82–96

    Article  CAS  PubMed  Google Scholar 

  • Kuroiwa T (1985) Mechanisms of maternal inheritance of chloroplast DNA: an active digestion hypothesis. Microbiol Sci 2:267–270

    CAS  PubMed  Google Scholar 

  • Kuroiwa T (1991) The replication, differentiation and inheritance of plastids with emphasis on the concept of organelle nuclei. Int Rev Cytol 128:1–62

    Article  CAS  Google Scholar 

  • Kuroiwa T, Suzuki T, Ogawa K, Kawano S (1981) The chloroplast nucleus: distribution, number, size, and shape, and a model for the multiplication of the chloroplast genome during chloroplast development. Plant Cell Physiol 22:381–396

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Matagne RF, Michel-Wolwertz MR, Munaut C, Duyckaerts C, Sluse F (1989) Induction and characterization of mitochondrial DNA mutants in Chlamydomonas reinhardtii. J Cell Biol 108:1221–1226

    Article  CAS  PubMed  Google Scholar 

  • Nakamura S, Aoyama H, Van-Woesik R (2003) Strict paternal transmission of mitochondrial DNA of Chlamydomonas species is explained by selection against maternal nucleoids. Protoplasma 221:205–210

    Article  CAS  PubMed  Google Scholar 

  • Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77:212–216

    Article  Google Scholar 

  • Nishimura Y, Higashiyama T, Suzuki L, Misumi O, Kuroiwa T (1998) The biparental transmission of the mitochondrial genome in Chlamydomonas reinhardtii visualized in living cells. Eur J Cell Biol 77:124–133

    CAS  PubMed  Google Scholar 

  • Remacle C, Bovie C, Michel-Wolwertz MR, Loppes R, Matagne RF (1990) Mitochondrial genome transmission in Chlamydomonas diploids obtained by sexual crosses and artificial fusions: role of the mating type and of a 1 kb intron. Mol Gen Genet 223:180–184

    Article  CAS  PubMed  Google Scholar 

  • Royer HD, Sager R (1979) Methylation of chloroplast DNAs in the life cycle of Chlamydomonas. Proc Natl Acad Sci USA 76:5794–5798

    Article  CAS  PubMed  Google Scholar 

  • Ryan R, Grant D, Chiang KS, Swift H (1978) Isolation and characterization of mitochondrial DNA from Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 75:3268–3272

    Article  CAS  PubMed  Google Scholar 

  • Sager R (1954) Mendelian and non-Mendelian inheritance of streptomycin resistance in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 40:356–363

    Article  CAS  PubMed  Google Scholar 

  • Sager R, Lane D (1972) Molecular basis of maternal inheritance. Proc Natl Acad Sci USA 69:2410–2413

    Article  CAS  PubMed  Google Scholar 

  • Sager R, Ramanis Z (1967) Biparental inheritance of nonchromosomal genes induced by ultraviolet irradiation. Proc Natl Acad Sci USA 58:931–937

    Article  CAS  PubMed  Google Scholar 

  • Sano H, Grabowy C, Sager R (1981) Differential activity of DNA methyltransferase in the life cycle of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 78:3118–3122

    Article  CAS  PubMed  Google Scholar 

  • Tilney-Bassett RAE (1978) The inheritance and genetic behaviour of plastids. In: Kirk JTO, Tilney-Bassett RAE (eds) The plastids: their chemistry, structure, growth and inheritance. Elsevier/North-Holland Biomedical, New York, pp 251–521

    Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research A to T.K. (No. 19207004) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. I am grateful to Dr. J.D. Reimer for a reading of the manuscript.

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Correspondence to Soichi Nakamura.

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Nakamura, S. Paternal inheritance of mitochondria in Chlamydomonas . J Plant Res 123, 163–170 (2010). https://doi.org/10.1007/s10265-009-0295-8

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  • DOI: https://doi.org/10.1007/s10265-009-0295-8

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