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. 1997 Sep;63(9):3426–3431. doi: 10.1128/aem.63.9.3426-3431.1997

Mitochondrial Haplotype Influences Mycelial Growth of Agaricus bisporus Heterokaryons

P Y De La Bastide, A Sonnenberg, L Van Griensven, J B Anderson, P A Horgen
PMCID: PMC1389239  PMID: 16535683

Abstract

We evaluated the influence of mitochondrial haplotype on growth of the common button mushroom Agaricus bisporus. Ten pairs of heterokaryon strains, each pair having the same nuclear genome but different mitochondrial genomes, were produced by controlled crosses among a group of homokaryons of both wild and commercial origins. Seven genetically distinct mitochondrial DNA (mtDNA) haplotypes were evaluated in different nuclear backgrounds. The growth of heterokaryon pairs differing only in their mtDNA haplotypes was compared by measuring mycelial radial growth rate on solid complete yeast medium (CYM) and compost extract medium and by measuring mycelial dry weight accumulation in liquid CYM. All A. bisporus strains were incubated at temperatures similar to those utilized in commercial production facilities (18, 22, and 26(deg)C). Statistically significant differences were detected in 8 of the 10 heterokaryon pairs evaluated for one or two of the three growth parameters measured. Some heterokaryon pairs showed differences in a single growth parameter at all three temperatures of incubation, suggesting a temperature-independent difference. Others showed differences at only a single temperature, suggesting a temperature-dependent difference. The influence of some mtDNA haplotypes on growth was dependent on the nuclear genetic background. Our results show that mtDNA haplotype can influence growth of A. bisporus heterokaryons in some nuclear backgrounds. These observations demonstrate the importance of including a number of mitochondrial genotypes and evaluating different nuclear-mitochondrial combinations of A. bisporus in strain improvement programs.

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Selected References

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  1. Attardi G., Schatz G. Biogenesis of mitochondria. Annu Rev Cell Biol. 1988;4:289–333. doi: 10.1146/annurev.cb.04.110188.001445. [DOI] [PubMed] [Google Scholar]
  2. Ballard J. W., Kreitman M. Unraveling selection in the mitochondrial genome of Drosophila. Genetics. 1994 Nov;138(3):757–772. doi: 10.1093/genetics/138.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Castle A. J., Horgen P. A., Anderson J. B. Crosses among Homokaryons from Commercial and Wild-Collected Strains of the Mushroom Agaricus brunnescens (= A. bisporus). Appl Environ Microbiol. 1988 Jul;54(7):1643–1648. doi: 10.1128/aem.54.7.1643-1648.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark A. G., Lyckegaard E. M. Natural selection with nuclear and cytoplasmic transmission. III. Joint analysis of segregation and mtDNA in Drosophila melanogaster. Genetics. 1988 Mar;118(3):471–481. doi: 10.1093/genetics/118.3.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Costanzo M. C., Fox T. D. Control of mitochondrial gene expression in Saccharomyces cerevisiae. Annu Rev Genet. 1990;24:91–113. doi: 10.1146/annurev.ge.24.120190.000515. [DOI] [PubMed] [Google Scholar]
  6. Garber R. C., Yoder O. C. Isolation of DNA from filamentous fungi and separation into nuclear, mitochondrial, ribosomal, and plasmid components. Anal Biochem. 1983 Dec;135(2):416–422. doi: 10.1016/0003-2697(83)90704-2. [DOI] [PubMed] [Google Scholar]
  7. Griffiths A. J. Fungal senescence. Annu Rev Genet. 1992;26:351–372. doi: 10.1146/annurev.ge.26.120192.002031. [DOI] [PubMed] [Google Scholar]
  8. Grivell L. A. Nucleo-mitochondrial interactions in mitochondrial gene expression. Crit Rev Biochem Mol Biol. 1995;30(2):121–164. doi: 10.3109/10409239509085141. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Hudspeth M. E., Shumard D. S., Tatti K. M., Grossman L. I. Rapid purification of yeast mitochondrial DNA in high yield. Biochim Biophys Acta. 1980 Dec 11;610(2):221–228. doi: 10.1016/0005-2787(80)90003-9. [DOI] [PubMed] [Google Scholar]
  11. Hutter C. M., Rand D. M. Competition between mitochondrial haplotypes in distinct nuclear genetic environments: Drosophila pseudoobscura vs. D. persimilis. Genetics. 1995 Jun;140(2):537–548. doi: 10.1093/genetics/140.2.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jin T., Horgen P. A. Further characterization of a large inverted repeat in the mitochondrial genomes of Agaricus bisporus (= A. brunnescens) and related species. Curr Genet. 1993 Mar;23(3):228–233. doi: 10.1007/BF00351501. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Kilpatrick S. T., Rand D. M. Conditional hitchhiking of mitochondrial DNA: frequency shifts of Drosophila melanogaster mtDNA variants depend on nuclear genetic background. Genetics. 1995 Nov;141(3):1113–1124. doi: 10.1093/genetics/141.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. King M. P., Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science. 1989 Oct 27;246(4929):500–503. doi: 10.1126/science.2814477. [DOI] [PubMed] [Google Scholar]
  17. Li A., Begin M., Kokurewicz K., Bowden C., Horgen P. A. Inheritance of Strain Instability (Sectoring) in the Commercial Button Mushroom, Agaricus bisporus. Appl Environ Microbiol. 1994 Jul;60(7):2384–2388. doi: 10.1128/aem.60.7.2384-2388.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nachman M. W., Boyer S. N., Aquadro C. F. Nonneutral evolution at the mitochondrial NADH dehydrogenase subunit 3 gene in mice. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6364–6368. doi: 10.1073/pnas.91.14.6364. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rand D. M., Dorfsman M., Kann L. M. Neutral and non-neutral evolution of Drosophila mitochondrial DNA. Genetics. 1994 Nov;138(3):741–756. doi: 10.1093/genetics/138.3.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Singh M., Hamel N., Menassa R., Li X. Q., Young B., Jean M., Landry B. S., Brown G. G. Nuclear genes associated with a single Brassica CMS restorer locus influence transcripts of three different mitochondrial gene regions. Genetics. 1996 May;143(1):505–516. doi: 10.1093/genetics/143.1.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wallace D. C. Mitochondrial DNA sequence variation in human evolution and disease. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8739–8746. doi: 10.1073/pnas.91.19.8739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Zolan M. E., Pukkila P. J. Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol. 1986 Jan;6(1):195–200. doi: 10.1128/mcb.6.1.195. [DOI] [PMC free article] [PubMed] [Google Scholar]

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