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. 1997 Dec;63(12):4686–4691. doi: 10.1128/aem.63.12.4686-4691.1997

Genetic evidence for nonrandom sorting of mitochondria in the basidiomycete Agrocybe aegerita.

G Barroso 1, J Labarère 1
PMCID: PMC168790  PMID: 9406387

Abstract

We studied mitochondrial transmission in the homobasidiomycete Agrocybe aegerita during plasmogamy, vegetative growth, and basidiocarp differentiation. Plasmogamy between homokaryons from progeny of three wild-type strains resulted in bidirectional nuclear migration, and the dikaryotization speed was dependent on the nuclear genotype of the recipient homokaryon. Little mitochondrial migration accompanied the nuclear migration. A total of 75% of the dikaryons from the fusion lines had both parental mitochondrial haplotypes (mixed dikaryons), and 25% had only a single haplotype (homoplasmic dikaryons); with some matings, there was a strong bias in favor of one parental haplotype. We demonstrated the heteroplasmic nature of mixed dikaryons by (i) isolating and subculturing apical cells in micromanipulation experiments and (ii) identifying recombinant mitochondrial genomes. This heteroplasmy is consistent with the previously reported suggestion that there is recombination between mitochondrial alleles in A. aegerita. Conversion of heteroplasmons into homoplasmons occurred (i) during long-term storage, (ii) in mycelia regenerated from isolated apical cells, and (iii) during basidiocarp differentiation. Homokaryons that readily accepted foreign nuclei were the most efficient homokaryons in maintaining their mitochondrial haplotype during plasmogamy, long-term storage, and basidiocarp differentiation. This suggests that the mechanism responsible for the nonrandom retention or elimination of a given haplotype may be related to the nuclear genotype or the mitochondrial haplotype or both.

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Selected References

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  1. BEISSON-SCHECROUN J. [Cellular incompatibility and nucleo-cytoplasmic interactions in the "barrage" phenomena in Podospora anserina]. Ann Genet. 1962;4:4–50. [PubMed] [Google Scholar]
  2. Barroso G., Blesa S., Labarere J. Wide Distribution of Mitochondrial Genome Rearrangements in Wild Strains of the Cultivated Basidiomycete Agrocybe aegerita. Appl Environ Microbiol. 1995 Apr;61(4):1187–1193. doi: 10.1128/aem.61.4.1187-1193.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birky C. W., Jr Relaxed cellular controls and organelle heredity. Science. 1983 Nov 4;222(4623):468–475. doi: 10.1126/science.6353578. [DOI] [PubMed] [Google Scholar]
  4. Birky C. W., Jr Transmission genetics of mitochondria and chloroplasts. Annu Rev Genet. 1978;12:471–512. doi: 10.1146/annurev.ge.12.120178.002351. [DOI] [PubMed] [Google Scholar]
  5. Boynton J. E., Harris E. H., Burkhart B. D., Lamerson P. M., Gillham N. W. Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2391–2395. doi: 10.1073/pnas.84.8.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fukuda M., Harada Y., Imahori S., Fukumasa-Nakai Y., Hayashi Y. Inheritance of mitochondrial DNA in sexual crosses and protoplast cell fusions in Lentinula edodes. Curr Genet. 1995 May;27(6):550–554. doi: 10.1007/BF00314446. [DOI] [PubMed] [Google Scholar]
  7. Hintz W., Anderson J. B., Horgen P. A. Nuclear migration and mitochondrial inheritance in the mushroom agaricus bitorquis. Genetics. 1988 May;119(1):35–41. doi: 10.1093/genetics/119.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Jin T., Horgen P. A. Uniparental Mitochondrial Transmission in the Cultivated Button Mushroom, Agaricus bisporus. Appl Environ Microbiol. 1994 Dec;60(12):4456–4460. doi: 10.1128/aem.60.12.4456-4460.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jin T., Sonnenberg A. S., Van Griensven L. J., Horgen P. A. Investigation of Mitochondrial Transmission in Selected Matings between Homokaryons from Commercial and Wild-Collected Isolates of Agaricus bisporus (= Agaricus brunnescens). Appl Environ Microbiol. 1992 Nov;58(11):3553–3560. doi: 10.1128/aem.58.11.3553-3560.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Labarère J., Noël T. Mating type switching in the tetrapolar basidiomycete Agrocybe aegerita. Genetics. 1992 Jun;131(2):307–319. doi: 10.1093/genetics/131.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lee S. B., Taylor J. W. Uniparental inheritance and replacement of mitochondrial DNA in Neurospora tetrasperma. Genetics. 1993 Aug;134(4):1063–1075. doi: 10.1093/genetics/134.4.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Matsumoto T., Fukumasa-Nakai Y. Mitochondrial DNA inheritance in sexual crosses of Pleurotus ostreatus. Curr Genet. 1996 Dec;30(6):549–552. doi: 10.1007/s002940050168. [DOI] [PubMed] [Google Scholar]
  13. May G., Taylor J. W. Patterns of mating and mitochondrial DNA inheritance in the agaric Basidiomycete Coprinus cinereus. Genetics. 1988 Feb;118(2):213–220. doi: 10.1093/genetics/118.2.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mogensen H. L. Exclusion of male mitochondria and plastids during syngamy in barley as a basis for maternal inheritance. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2594–2597. doi: 10.1073/pnas.85.8.2594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Moulinier T., Barroso G., Labarère J. The mitochondrial genome of the basidiomycete Agrocybe aegerita: molecular cloning, physical mapping and gene location. Curr Genet. 1992 May;21(6):499–505. doi: 10.1007/BF00351660. [DOI] [PubMed] [Google Scholar]
  16. Smith M. L., Duchesne L. C., Bruhn J. N., Anderson J. B. Mitochondrial genetics in a natural population of the plant pathogen armillaria. Genetics. 1990 Nov;126(3):575–582. doi: 10.1093/genetics/126.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  18. Specht C. A., Novotny C. P., Ullrich R. C. Mitochondrial DNA of Schizophyllum commune: restriction map, genetic map, and mode of inheritance. Curr Genet. 1992 Aug;22(2):129–134. doi: 10.1007/BF00351472. [DOI] [PubMed] [Google Scholar]
  19. Zouros E., Freeman K. R., Ball A. O., Pogson G. H. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature. 1992 Oct 1;359(6394):412–414. doi: 10.1038/359412a0. [DOI] [PubMed] [Google Scholar]
  20. Zweifel S. G., Fangman W. L. A nuclear mutation reversing a biased transmission of yeast mitochondrial DNA. Genetics. 1991 Jun;128(2):241–249. doi: 10.1093/genetics/128.2.241. [DOI] [PMC free article] [PubMed] [Google Scholar]

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