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Mitochondrial inheritance in filamentous fungi

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Abstract

Because of the ease with which fungal strains and life cycles can be manipulated, fungal research has made important contributions to the present understanding of mitochondrial inheritance generally. Several mitochondrial DNA molecules have been completely sequenced and this information has provided useful probes for study of other mitochondrial genomes. Mapping and sequencing has shown that the mtDNA is circular, butin vivo many linear derivatives are observed whose significance is unclear. The genes carried in mtDNA are for components of the electron transport system, ATP synthesis and mitochondrial protein synthesis. Multigenic transcripts are processed to arrive at mRNAs. The mitochondrial genetic code shows several differences compared to the universal code. MtDNA shows a high level of neutral variation due to length mutations and restriction site differences: these are useful in measuring genetic distances in evolutionary and taxonomic studies. Mutations affecting gene function lead to slow/erratic growth or drug resistance. Many mutations are suppressive, rapidly dominating the culture. Mitochondrial plasmids are common in natural isolates of fungi. Strains can contain mixtures of linear and circular types. Some plasmid families show widespread distribution, across different species and genera. Linear plasmids generally have genes for presumptive DNA and RNA polymerases. Circular plasmids have a single gene for a DNA polymerase or a reverse transcriptase. Several plasmids recombine with mtDNA; the most striking cases are the senescence plasmids, which integrate into mtDNA and cause death through insertional mutagenesis. Genetic elements in the mitochondria, and the phenotypes determined by them, are inherited maternally or uniparentally in sexual crosses. Mitochondrial elements and phenotypes are transmitted by cytoplasmic contact between cells. In heteroplasmons the mitochondrial mixtures often segregate during somatic propagation, resulting in pure derivatives. Heteroplasmons also offer the opportunity for recombination between different mtDNA molecules.

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References

  • Akins R. A., Kelley R. L. and Lambowitz A. M. 1986 Mitochondrial plasmids ofNeurospora: integration into mitochondrial DNA and evidence for reverse transcription in mitochondria.Cell 47: 505–516

    Article  Google Scholar 

  • Appel D. J. and Gordon T. R. 1995 Intraspecific variation within populations ofFusarium oxysporum based on RFLP analysis of the intergenic spacer region of the rDNA.Exp. Mycol. 19: 120–128

    Article  Google Scholar 

  • Beattie T. L., Olive J. E. and Collins R. A. 1995 A secondary structure model for the self-cleaving region of the Neurospora VS RNA.Proc. Natl. Acad. Sci. USA 92: 4686–4690

    Article  PubMed  CAS  Google Scholar 

  • Belcour L. and Begel O. 1977 Mitochondrial genes inPodospora anserina: recombination and linkage.Mol. Gen. Genet. 153: 11–21

    Article  PubMed  CAS  Google Scholar 

  • Bendich A. J. 1993 Reaching for the ring: the study of mitochondrial genome structure.Curr. Genet. 24: 279–290

    Article  PubMed  CAS  Google Scholar 

  • Bertrand H. 1995 Senescence is coupled to induction of an oxidative phosphorylation stress response by mitochondrial DNA mutations inNeurospora.Can. J. Bot. 73: S198-S204

    Article  Google Scholar 

  • Birky C. W. 1983 Relaxed cellular controls and organelle heredity.Science 222: 468–475

    Article  PubMed  Google Scholar 

  • Bridge P. D., Hopkinson L. A. and Rutherford M. A. 1995 Rapid mitochondrial probes for analysis of polymorphisms inFusarium oxysporum special forms.Lett. Appl. Microbiol. 21: 198–201

    Article  PubMed  CAS  Google Scholar 

  • Bruns T. D. and Palmer J. D. 1989 Evolution of mushroom mitochondrial DNA:Suillus and related genera.J. Mol. Evol. 28: 349–362

    Article  PubMed  CAS  Google Scholar 

  • Carvalho D. B., Smith M. L. and Anderson J. B. 1995 Genetic exchange between diploid and haploid mycelia ofArmillaria gallica.Mycol. Res. 99: 641–647

    Google Scholar 

  • Caten C. E. 1972 Vegetative incompatibility and cytoplasmic infection in fungi.J. Gen. Microbiol. 72: 221–229

    PubMed  CAS  Google Scholar 

  • Cech T. R. 1990 Self-splicing of group I introns.Annu. Rev. Biochem. 59: 543–568

    Article  PubMed  CAS  Google Scholar 

  • Coenen A., Croft J. H., Slakhorst M., Debets F. and Hoekstra R. 1996 Mitochondrial inheritance inAspergillus nidulans.Genet. Res. 67: 93–100

    PubMed  CAS  Google Scholar 

  • Collins R. A. and Lambowitz A. M. 1983 Structural variations and optional introns in the mitochondrial DNAs ofNeurospora strains isolated from nature.Plasmid 9: 53–70

    Article  PubMed  CAS  Google Scholar 

  • Correll J. C., Rhoades D. D. and Guerber J. C. 1993 Examination of mitochondrial DNA restriction length polymorphisms, DNA fingerprints, and randomly amplified polymorphic DNA ofColletotrichum orbiculare.Phytopathology 83: 1198–1204

    Article  Google Scholar 

  • Debets F., Yang X. and Griffiths A. J. F. 1994 Vegetative incompatibility inNeurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations.Curr. Genet. 26: 113–119

    Article  PubMed  CAS  Google Scholar 

  • Esser K., Kuck U., Lang-Hinrichs C., Lemke P., Osiewacz H. D., Stahl U. and Tudzynski P. 1986Plasmids of eukaryotes. Fundamentals and applications (New York: Springer-Verlag)

    Google Scholar 

  • Fincham J. R. S., Day P. R. and Radford A. 1979Fungal genetics, 4th edn (Oxford: Blackwell)

    Google Scholar 

  • Fischer M. and Seefelder S. 1995 Mitochondrial DNA and its inheritance inPleurotus ostreatus andP. pulmonarius.Bot. Acta 108: 334–343

    CAS  Google Scholar 

  • Fukuda M., Harada Y., Irnahori S., Fukumasa-Nakai Y. and Hayashi Y. 1995 Inheritance of mitochondrial DNA in sexual crosses and protoplast cell fusions inLentinula edodes.Curr. Genet. 27: 550–554

    Article  PubMed  CAS  Google Scholar 

  • Gillham N. W. 1994Organelle genes and genomes (New York: Oxford University Press)

    Google Scholar 

  • Griffiths A. J. F. 1992 Fungal senescence.Annu. Rev. Genet. 26: 351–372

    Article  PubMed  CAS  Google Scholar 

  • Griffiths A. J. F. 1995 Natural plasmids of filamentous fungi.Microbiol. Rev. 59: 673–685

    PubMed  CAS  Google Scholar 

  • Griffiths A. J. F. and Yang X. 1995 Recombination between heterologous linear and circular mitochondrial plasmids in the fungusNeurospora.Mol. Gen. Genet. 249: 25–36

    Article  PubMed  CAS  Google Scholar 

  • Griffiths A. J. F., Collins, R. A. and Narang F. E. 1995 The mitochondrial genetics ofNeurospora. InThe Mycota II. Genetics and biotechnology (ed.) U. Kück (Heidelberg: Springer-Verlag)

    Google Scholar 

  • Hawse A., Collins R. A. and Nargang F. E. 1990 Behaviour of the [mi-3] mutation and conversion of polymorphic mtDNA markers in heterokaryons ofNeurospora crassa.Genetics 126: 63–72

    PubMed  CAS  Google Scholar 

  • Hermanns J. and Osiewacz H. D. 1994 Three mitochondrial unassigned open reading frames ofPodospora anserina represent remnants of a viral-type RNA polymerase gene.Curr. Genet. 25: 150–157

    Article  PubMed  CAS  Google Scholar 

  • Jin T. and Horgen P. A. 1994 Uniparental mitochondrial transmission in the cultivated button mushroomAgaricus bisporus.Appl. Environ. Microbiol. 60: 4456–4460

    PubMed  CAS  Google Scholar 

  • Kempken F. 1995a Plasmid DNA in mycelial fungi. InThe Mycota II. Genetics and biotechnology, (ed.) U. Kück (Heidelberg: Springer-Verlag)

    Google Scholar 

  • Kempken F. 1995b Horizontal gene transfer of a mitochondrial plasmid.Mol. Gen. Genet. 248: 89–94

    Article  PubMed  CAS  Google Scholar 

  • Kubelik A. R., Kennell J. C., Akins R. A. and Lambowitz A. M. 1990 Identification ofNeurospora mitochondrial promoters and analysis of synthesis of the mitochondrial small rRNA in wild-type and the promoter mutant [poky].J. Biol. Chem. 265: 4515–4526

    PubMed  CAS  Google Scholar 

  • Kukuda M., Nakai Y. E., Hibbett D. S., Matsumoto T. and Hayashi Y. 1994 Mitochondrial DNA restriction fragment length polymorphism in natural populations ofLentinus edodes.Mycol. Res. 98: 169–175

    Article  Google Scholar 

  • Kurdyla T. M., Guthrie P. A. I., McDonald B. A. and Appel D. N. 1995 RFLPs in mitochondrial and nuclear DNA indicate low levels of genetic diversity in the oak wilt pathogenCeratocystis fagacearum.Curr. Genet. 27: 373–378

    Article  PubMed  CAS  Google Scholar 

  • Lambowitz A. M. 1989 Infectious introns.Cell 56: 323–326

    Article  PubMed  CAS  Google Scholar 

  • Lee S. B. and Taylor J. W. 1993 Uniparental inheritance and replacement of mitochondrial DNA inNeurospora tetrasperma.Genetics 134: 1063–1075

    PubMed  CAS  Google Scholar 

  • Manella C. A. and Lambowitz A. M. 1979 Unidirectional gene conversion associated with two insertions inNeurospora crassa mitochondrial DNA.Genetics 93: 645–654

    Google Scholar 

  • Marcou D. 1961 Notion de longevite et nature cytoplasmique du determinant de sénescence chez quelques champignons.Ann. Sci. Nat. Bot. 11: 653–764

    Google Scholar 

  • Matsumoto T. and Fukumasa-Nakai Y. 1993 Mitochondrial DNA polymorphism and inheritance inLentinula edodes andPleurotus ostreatus.Rep. Tottori Mycol. Inst. 13: 153–161

    Google Scholar 

  • Matsumoto T. and Fukumasa-Nakai Y. 1994 Isolation and genetic analysis of a chloramphenicol-resistant mutant ofPleurotus ostreatus.Biosci. Biotechnol. Biochem. 58: 434–435

    CAS  Google Scholar 

  • Michel F. and Ferat J. L. 1995 Structure and activity of group II introns.Annu. Rev. Biochem. 64: 435–461

    Article  PubMed  CAS  Google Scholar 

  • Milgroom M. G. and Lipari S. E. 1995 Spatial analysis of nuclear and mitochondrial RFLP genotypes in populations of chestnut blight fungusCryphonectria parasitica.Mol. Ecol. 4: 633–642

    Article  PubMed  CAS  Google Scholar 

  • Osiewacz H. D. 1996 Extrachromosomal and transposable elements. InFungal genetics: principles and practice. (ed.) C. J. Bos (New York: Marcel Dekker)

    Google Scholar 

  • Robison M. M. and Horgen P. A. 1996 Plasmid RNA polymerase-like mitochondrial sequences inAgaricus bitorquis.Curr. Genet. 29: 37–376

    Article  Google Scholar 

  • Robison M. M., Royer J. C. and Horgen P. A. 1991 Homology between mitochondrial DNA ofAgaricus bisporus and an internal portion of a linear mitochondrial plasmid ofAgaricus bitorquis.Curr. Genet. 19: 495–502

    Article  PubMed  CAS  Google Scholar 

  • Sainsard-Chanet A., Begel O. and Belcour L. 1994 DNA double-strand break in vivo at the 3’ extremity of exons located upstream of group II introns: senescence and circular DNA introns inPodospora mitochondria.J. Mol. Biol. 242: 630–643

    Article  PubMed  CAS  Google Scholar 

  • Saldanha R. J., Patel S. S., Surendran R., Lee J. C. and Lambowitz A. M. 1995 Involvement ofNeurospora mitochondrial tyrosyl-tRNA synthetase in RNA splicing: a new method for purifying the protein and characterization of physical and enzymatic properties pertinent to splicing.Biochemistry 34: 1275–1287

    Article  PubMed  CAS  Google Scholar 

  • Sellem C. H., Lecellier G. and Belcour L. 1993 Transposition of a group II intron.Nature 366: 176–178

    Article  PubMed  CAS  Google Scholar 

  • Smith M. L., Bruhn J. H. and Anderson J. B. 1994 Relatedness and spatial distribution ofArmillaria genets infecting red pine seedlings.Phytopathology 84: 822–829

    Article  Google Scholar 

  • Taylor J. W. 1986 Fungal evolutionary biology and mitochondrial DNA.Exp. Mycol. 10: 259–269

    Article  CAS  Google Scholar 

  • Taylor J. W. and Lobuglio K. F. 1994 Ascomycete phylogenetics: morphology and evolution.Mycoscience 35: 109–112

    Article  Google Scholar 

  • Van Horn R. and Clay K. 1995 Mitochondrial DNA variation in the fungusAtkinsonella hypoxylon infecting sympatricDanthonia grasses.Evolution 49: 360–371

    Article  Google Scholar 

  • Varga J., Kevei F., Vriesema A., Debets F., Kozakiewicz Z. and Croft J. H. 1994 Mitochondrial DNA restriction fragment length polymorphisms in field isolates of theAspergillus niger aggregate.Can J. Microbiol. 40: 612–621

    Article  PubMed  CAS  Google Scholar 

  • Vicente M. J., Abad P. and Cenis J. L. 1994 RFLPs of mitochondrial DNA, RAPDs and VCGs ofAcremonium sp: genetic markers for the taxonomic identification.Investigation Agraria Production y Protection vegetales suppl. 2: 401–416

    Google Scholar 

  • Wolf K. and Del Giudice L. 1988 The variable mitochondrial genome of ascomycetes: organization, mutational alterations and expression.Adv. Genet. 25: 185–308

    Article  PubMed  CAS  Google Scholar 

  • Yang X. and Griffiths A. J. F. 1993 Plasmid suppressors active in the sexual cycle ofNeurospora intermedia.Genetics 135: 993–1002

    PubMed  CAS  Google Scholar 

  • Yates-Siliata K. E., Sander D. M. and Keath E. J. 1995 Genetic diversity in clinical isolates of the dimorphic fungusBlastomyces dermatiditis detected by a PCR-based random amplified polymorphic DNA assay.J. Clin. Microbiol. 33: 2171–2175

    Google Scholar 

  • Yuewang W., Yang X. and Griffiths A. J. F. 1995 Structure of aGelasinospora linear plasmid closely related to the kalilo plasmid ofNeurospora intermedia.Curr. Genet. 29: 150–158

    Google Scholar 

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  1. Department of Botany, University of British Columbia, V6T 1Z4, Vancouver, B.C., Canada

    Anthony J. F. Griffiths

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Griffiths, A.J.F. Mitochondrial inheritance in filamentous fungi. J. Genet. 75, 403–414 (1996). https://doi.org/10.1007/BF02966318

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