Skip to main content
SpringerLink
Log in

Mitochondrial morphogenesis and ultrastructure of basidiomycetes from genera Agaricus and Pleurotus

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

Supravital study of rhodamine-stained mitochondria in cells of aerial and submerged micelium of 31 strains from 9 species from genus Agaricus (A. arvensis Schaeff., A. bisporus (Lange) Imbach, A. bitorquis (Quel.) Sacc., A. campestris L., A. excellens, (F.H. Müller) F.H. Müller, A. macrocarpus (F.H. Müller) F.H. Müller, A. silvaticus Schaeff., A. silvicola (Vittad.) Peck, A. xanthodermus Genev) and of 2 strains from 2 species from genus Pleurotus (P. ostreatus (Jacg.) P. Kumm., P. pulmonarius (Fr.) Quel.) was carried out. Mitochondrial morphogenesis in micelial cells of species from Agaricus and Pleurotus genera has many common features in distribution of mitochondria in micelial cells both under the favorable growth conditions and during chondriom reorganization (fission and fragmentation of mitochondria to small subunits) under unfarovable growth conditions and during aging. During the balanced growth of mycelium of heterokaryotic strains from genera Agaricus and Pleurotus for 7–14 days on agar media as well as during cultivation of mycelium of oyster mushroom and several strains of field mushroom in submerged culture, distribution of mitochondria by the type 1 (small granular mitochondria in the apical zone—1, long rod-like mitochondria in the subapical zone—2 and short rod-like and granular mitochondria formed as a result of fragmentation of rod-like mitochondria in mature mycelium cells—3) was observed. Under unfarovable growth conditions (starvation), in mycelium cells of homokaryotic strains of champignon, during long cultivation of all strains and species from the studied genera and during cultivation on liquid wort, for majority of champignon, distribution of mitochondria by the type 2 was observed (sphere-like mitochondria in all cells of the studied mycelium zones). Mitochondrial profiles at ultrastructural level had specific features, such as associations of the outer mitochondrial membrane with cytoplasmic ribosomes and changes in cristae structure. The preliminary test for apoptosis-like phenotype of the submerged mycelium cells of Bs94 champignon that hardly grows in the submerged culture gave positive result. Thus, mitochondrial morphogenesis in mycelium cells of Agaricus and Pleurotus species under different conditions and terms of cultivation occurs similarly and is determined by a complex of physiological and biochemical processes reflecting the state of mycelium cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ades, I.Z and Butow, R.A., The Transport of Protein into Yeast Mitochondria, J. Biol. Chem., 1980, vol. 255. pp. 9925–9935.

    PubMed  CAS  Google Scholar 

  • Almann K. and Westermann, B., Role of Essential Genes in Mitochondrial Morphogenesis in Saccharomyces cesevisiae, Mol. Biol. Cell, 2005, vol. 16, pp. 5410–5417.

    Article  CAS  Google Scholar 

  • Belcour, L., Mitochnondrial DNA and Senescence in Podospora anserine, Curr. Genet., 1981, vol. 4, pp. 81–82.

    Article  CAS  Google Scholar 

  • Borghouts, C., Kimpel, E., and Osiewacz, H.D., Mitochondrial DNA Rearrangements of Podospora anserine Are under the Control of the Nuclear Gene grisea, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 10768–10773.

    Article  PubMed  CAS  Google Scholar 

  • Burgess, S.M., Delannoy, M., and Jensen, R.E., MMM1 Encodes a Mitochondrial Outer Membrane Protein Essential for Establishing and Maintaining the Structure of Yeast Mitochondria, J. Cell Biol., 1994, vol. 126, pp. 1375–1391.

    Article  PubMed  CAS  Google Scholar 

  • Butt, T.M., Hoch, H.C., Staples, R.C., and Leger, R.Y.S., Use of Fluorochromes in the Study of Fungal Cytology and Differentiation, Exp. Mycol., 1989, vol. 13, pp. 303–313.

    Article  CAS  Google Scholar 

  • Cotter, D.A., Miura-Santo, L.Y., and Hohl, H.R., Ultrastructural Changes during Germination of Dyctiostelium discoideum Spores, J. Bacteriol., 1969, vol. 100, pp. 1020–1026.

    PubMed  CAS  Google Scholar 

  • Cummings, D.J., Belcour, L., and Grandchamp, C., Mitochondrial DNA from Podospora anserine. II. Properties of Mutant DNA and Multimeric Circular DNA from Senescent Cultures, Mol. Gen. Genet., 1979, vol. 171, pp. 239–250.

    Article  PubMed  CAS  Google Scholar 

  • Desagher, S. and Martinou, J.C., Mitochondria as the Central Control Point of Apoptosis, Trends Cell Biol., 2000, vol. 10. pp. 369–377.

    Article  PubMed  CAS  Google Scholar 

  • Fünfschilling, U. and Rospert, S., Nascent Polypeptide-Associated Complex Stimulates Protein Import into Yeast Mitochondria, Mol. Biol. Cell, 1999, vol. 10, pp. 3289–3299.

    PubMed  Google Scholar 

  • Jamet-Vierny, C., Begel, O., and Belcour, L., Senescence in Podospora anserine: Amplification of a Mitochondrial DNA Sequence, Cell, 1980, vol. 21, pp. 189–194.

    Article  PubMed  CAS  Google Scholar 

  • Jamet-Vierny, C., Boulay, J., Begel, O., and Silar, P., Contribution of Various Classes of Defective Mitochondrial DNA Molecules to Senescence in Podospora anserine, Curr. Genet. 1999, vol. 27, pp. 26–35.

    CAS  Google Scholar 

  • Kamzolkina, O.V., Micromorphology and Ultrastructure of Agaricoid Fungi at Different Stages of Their Life Cycles, Doctoral (Biol.) Dissertation, Moscow: Mosk. Gos. Univ., 2005.

    Google Scholar 

  • Kellems, R.E. and Butow, R.A., Cytoplasmic-Type 80S Ribosomes Associated with Yeast Mitochondria. I. Evidence for Ribosome Binding Sites on Yeast Mitochondria, J. Biol. Chem., 1972, vol. 247, pp. 8043–8050.

    PubMed  CAS  Google Scholar 

  • Kellems, R.E. and Butow, R.A., Cytoplasmic-Type 80S Ribosomes Associated with Yeast Mitochondria. II. Changes in the Amount of Bound Ribosomes in Response to Changes in Metabolic State, J. Biol. Chem., 1974, vol. 249, pp. 3304–3310.

    PubMed  CAS  Google Scholar 

  • Kellems, R.E., Allison, V.F., and Butow, R.A., Cytoplasmic Type 80S Ribosomes Associated with Yeast Mitochondria. II. Evidence for the Association of Cytoplasmic Ribosomes with the Outer Mitochondrial Membrane, J. Biol. Chem., 1974, vol. 249, pp. 3297–3303.

    PubMed  CAS  Google Scholar 

  • Kellems, R.E., Allison, V.F., and Butow, R.A., Cytoplasmic Type 80S Ribosomes Associated with Yeast Mitochondria. IV. Attachment of Ribosomes to the Outer Membrane of Isolated Mitochnondria, J. Cell Biol., 1975, vol. 65, pp. 1–14.

    Article  PubMed  CAS  Google Scholar 

  • Keyhani, E., Ribosomal Granules Associated with Outer Mitochondrial Membrane in Aerobic Yeast Cells, J. Cell Biol., 1973, vol. 58, pp. 480–484.

    Article  PubMed  CAS  Google Scholar 

  • Knorre, D.A., Pheromone-Induced Programmed Cell Death of Saccharomyces cerevisiae, Cand. Sci. (Biol.) Dissertation, Moscow: Mosk. Gos. Univ., 2005.

    Google Scholar 

  • Kürk, U., Stahl, U., and Esser, K., Plasmid-Like DNA Is Part of the Mitochondrial DNA in Podospora anserine, Curr. Genet., 1981, vol. 3, pp. 151–156.

    Article  Google Scholar 

  • Lee, S.Y., Krsmanovic, V., and Brawerman, G., Attachment of Ribosomes to Membranes during Polysome Formation in Mouse Sarcoma 180 Cells, J. Cell Biol., 1971, vol. 49. pp. 683–691.

    Article  PubMed  CAS  Google Scholar 

  • Lewina, N.N. and Lew, R.R., The Role of Tip-Localized Mitochondria in Hyphal Growth, Fungal Genet. Biol., 2006. vol. 43, pp. 65–74.

    Article  CAS  Google Scholar 

  • Lill, R. and Mühlenhoff, U., Iron-Sulfur-Protein Biogenesis in Eukaryotes, Trends Biochem. Sci., 2005, vol. 30, pp. 133–141.

    Article  PubMed  CAS  Google Scholar 

  • Litvinov, M.A., Metody izucheniya pochvennykh mikroskopicheskikh gribov (Methods of Study of Soil Microscopic Fungi), Leningrad: Nauka, 1969.

    Google Scholar 

  • Loeb, J.N., Howell, R.R., and Tomkins, G.M., Free and Membrane-Bound Ribosomes in Rat Liver, J. Biol. Chem., 1967, vol. 242, pp. 2069–2074.

    PubMed  CAS  Google Scholar 

  • Lu, B.C., Programmed Cell Death, in Fungi. The Mycota. I. Growth Differentiation and Sexuality, 2006, pp. 167–187.

  • MacKenzie, J.A. and Payne, R.M., Ribosomes Specifically Bind to Mammalian Mitochondria via Protease-Sensitive Proteins on the Outer Membrane, J. Biol. Chem., 2004. vol. 279, pp. 9803–9810.

    Article  PubMed  CAS  Google Scholar 

  • Marcou, D., Notion de longetite et nature cytoplasmique du determinant de la senescence chez quelques champignons, Ann. Sci. Nat. Bot., 1961, vol. 12, pp. 653–764.

    Google Scholar 

  • Pelloquin, L., Belenguer, P., Menon, Y., and Ducommum, B., Identification of a Fusion Yeast Dynamic-Related Protein Involved in Mitochondrial DNA Maintenance, Biochem. Biophys. Res. Commun., 1998, vol. 251, pp. 720–726.

    Article  PubMed  CAS  Google Scholar 

  • Prokisch, H., Neupert, W., and Westermann, B., Role of MMM1 in Maintaining Mitochondrial Morphology in Neurospora crassa, Mol. Biol. Cell, 2000, vol. 11, pp. 2961–2971.

    PubMed  CAS  Google Scholar 

  • Reynolds, E.S., The Use of Lead Citrate at High pH as an Electron Opaque Strain in Electron Microscopy, J. Biophys. Biochem. Cytol., 1963, vol. 17, p. 208.

    Article  CAS  Google Scholar 

  • Rizet, D., Sur la longevite des souches de Podospora anserine, CR. Acad. Sci., 1953, vol. 237, pp. 1106–1109.

    CAS  Google Scholar 

  • Sellem, C.H., Dynamics of the Mitochondrial Genome during Podospora anserine Aging, Curr. Genet., 2002, vol. 40. pp. 365–373.

    Article  PubMed  CAS  Google Scholar 

  • Stahl, U., Lemke, P.A., Tudzynski, P., Kürk, U., and Esser, K., Evidence for Plasmid Like DNA in Filamentous Fungus, the Ascomycete Podospora anserine, Mol. Gen. Genet., 1978. vol. 162, pp. 341–343.

    Article  PubMed  CAS  Google Scholar 

  • Watson, K., The Organization of Ribosomal Granules within Mitochondrial Structures of Aerobic and Anaerobic Cells of Saccharomyces cerevisiae, J. Cell. Biol., 1972, vol. 55. pp. 721–726.

    Article  PubMed  CAS  Google Scholar 

  • Westermann, B. and Prokisch, H., Mitochondrial Dynamics in Filamentous Fungi, Fungal Genet. Biol., 2002, vol. 36. pp. 91–97.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Mycology and Algology Department, Biological Faculty, Moscow State University, Moscow, Russia

    E. V. Matrosova, I. S. Masheyka, O. A. Kudryavtseva & O. V. Kamzolkina

Authors
  1. E. V. Matrosova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. S. Masheyka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. O. A. Kudryavtseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. O. V. Kamzolkina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Kamzolkina.

Additional information

Original Russian Text © E.V. Matrosova, I.S. Masheyka, O.A. Kudryavtseva, O.V. Kamzolkina, 2009, published in Tsitologiya, Vol. 51, No. 6, 2009, pp. 490–499.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matrosova, E.V., Masheyka, I.S., Kudryavtseva, O.A. et al. Mitochondrial morphogenesis and ultrastructure of basidiomycetes from genera Agaricus and Pleurotus . Cell Tiss. Biol. 3, 369–380 (2009). https://doi.org/10.1134/S1990519X09040099

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X09040099

Keywords

Search

Navigation