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Abnormal meiosis in bisporic strains of white button mushroom Agaricus bisporus (Lange) imbach

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Abstract

A formerly developed method of microspreading of mushroom basidial nuclei was applied to study meiotic prophase I in bisporic white button mushroom (Agaricus bisporus) strains. Meiotic recombination and assemblage of axial structures (axial elements and synaptonemal complexes) of chromosomes in meiotic prophase I are interrelated. It is known that the frequency of meiotic recombination is reduced in the bisporic A. bisporus variety. We showed that formation of axial structures of meiotic chromosomes in bisporic strains of this mushroom was disrupted. The anomalous phenotypes in spread prophase nuclei are diverse. In leptotene and early zygotene, many nuclei contain abnormal, often short, and, as a rule, few chromosomal axial elements. The abnormalities in the formation of synaptonemal complexes at the zygotene-diplotene stage are of the same kind and even more pronounced. We discovered an important feature of meiosis in A. bisporus associated with fruit-body morphogenesis. Meiosis starting in basidia (meiocytes) of young closed fruit bodies is accompanied by disruption of chromatin condensation in prophase I and, probably, is arrested. After partial veil breakage, the course of meiosis normalizes. Preparations with clearly observable chromosomal axial structures can be obtained only at this stage of fruit-body development.

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References

  1. Bogdanov, Yu.F., Variation and Evolution of Meiosis, Rus. J. Genet., 2003, vol. 39, no. 4, pp. 363–381.

    Article  CAS  Google Scholar 

  2. Henderson, K.A. and Keeney, S., Tying Synaptonemal Complex Initiation to the Formation and Programmed Repair of DNA Double-Strand Breaks, Proc. Natl. Acad. Sci. USA, 2004, vol. 101, pp. 4519–4524.

    Article  CAS  PubMed  Google Scholar 

  3. Celerin, M., Merino, S.T., Stone, J.E., et al., Multiple Roles of Spo11 in Meiotic Chromosome Behavior, EMBO J., 2000, vol. 19, pp. 2739–2750.

    Article  CAS  PubMed  Google Scholar 

  4. Bhuiyan, H. and Schmekel, K., Meiotic Chromosome Synapsis in Yeast Can Occur without Spo11-Induced DNA Double-Strand Breaks, Genetics, 2004, vol. 168, pp. 775–783.

    Article  CAS  PubMed  Google Scholar 

  5. Haber, J.E., The Many Interfaces of Mre11, Cell (Cambridge, Mass.), 1998, vol. 95, pp. 583–586.

    CAS  Google Scholar 

  6. Gerecke, E.E. and Zolan, M.E., An mre11 Mutant of Coprinus cinereus Has Defects in Meiotic Chromosome Pairing, Condensation and Synapsis, Genetics, 2000, vol. 154, pp. 1125–1139.

    CAS  PubMed  Google Scholar 

  7. Heyting, C., Synaptonemal Complexes: Structure and Function, Curr. Biol. Cell Biol., 1996, vol. 8, pp. 389–396.

    CAS  Google Scholar 

  8. Schwarzacher, T., Meiosis, Recombination and Chromosomes: A Review of Gene Isolation and Fluorescent in Situ Hybridization Data in Plants, J. Exp. Bot., 2003, vol. 54, pp. 11–23.

    Article  CAS  PubMed  Google Scholar 

  9. Grishchuk, A.L. and Kohli, J., Five RecA-Like Proteins of Schizosaccharomyces pombe Are Involved in Meiotic Recombination, Genetics, 2003, vol. 165, pp. 1031–1048.

    CAS  PubMed  Google Scholar 

  10. Jiao, K., Salem, L., and Malone, R., Support for a Meiotic Recombination Initiation Complex: Interactions among Rec102p, Rec104p, and Spo11p, Mol. Cell. Biol., 2003, vol. 23, pp. 5928–5938.

    Article  CAS  PubMed  Google Scholar 

  11. Namekawa, S., Ichijima, Y., Hamada, F., et al., DNA Ligase IV from a Basidiomycete, Coprinus cinereus, and Its Expression during Meiosis, Microbiology, 2003, vol. 149, pp. 2119–2128.

    Article  CAS  PubMed  Google Scholar 

  12. Anuradna, S. and Muniyappa, K., Meiosis-Specific Yeast Hop1 Protein Promotes Synapsis of Double-Stranded DNA Helices Via the Formation of Guanine Quartets, Nucleic Acids Res., 2004, vol. 32, pp. 2378–2385.

    Google Scholar 

  13. Royse, D.J. and May, B., Use of Isozyme Variation to Identify Genotypic Classes of Agaricus brunnescens, Mycologia, 1982, vol. 74, pp. 93–102.

    CAS  Google Scholar 

  14. Castle, A.J., Horgen, P.A., and Anderson, J.B., Restriction Fragment Length Polymorphisms in the Mushrooms Agaricus brunnescens and Agaricus bitorquis, Appl. Environ. Microbiol., 1987, vol. 53, pp. 816–822.

    CAS  PubMed  Google Scholar 

  15. Summerbell, R.C., Castle, A.J., Horgen, P.A., and Anderson, J.B., Inheritance of Restriction Fragment Length Polymorphisms in Agaricus brunnescens, Genetics, 1989, vol. 123, pp. 293–300.

    CAS  PubMed  Google Scholar 

  16. Kerrigan, R.W., Royer, J.C., Baller, L.M., et al., Meiotic Behavior and Linkage Relationships in Secondary Homotallic Fungus Agaricus bisporus, Genetics, 1993, vol. 133, pp. 225–236.

    CAS  PubMed  Google Scholar 

  17. D’yakov, Yu.T., Fungal Reproduction Systems and Their Evolution, Mikol. Fitopatol., 1999, vol. 33, pp. 137–149.

    Google Scholar 

  18. Evans, H.J., Nuclear Behavior in the Cultivated Mushroom, Chromosoma, 1959, vol. 10, pp. 115–135.

    Article  CAS  PubMed  Google Scholar 

  19. Raper, C.A., Raper, J.R., and Miller, R.E., Genetic Analysis of the Life-Cycle of Agaricus bisporus, Mycologia, 1972, vol. 64, pp. 1088–1117.

    Google Scholar 

  20. Elliott, T.J., Breedeng Strategies in Agaricus bisporus, Mush. Sci., 1979, vol. 10, pp. 73–81.

    Google Scholar 

  21. Callac, P., Billette, C., Imbernon, M., and Kerrigan, R., Morphological, Genetic and Interfertility Analyses Reveal a Novel, Tetrasporic Variety of Agaricus bisporus from the Sonoran Desert of California, Mycologia, 1993, vol. 89, no. 5, pp. 835–851.

    Google Scholar 

  22. Imbernon, M.P., Callac, P., Gasqui, P., et al., BSN, the Primary Determinant of Basidial Spore Number and Reproductive Mode in Agaricus bisporus, Maps to Chromosome I, Mycologia, 1996, vol. 88, pp. 749–761.

    CAS  Google Scholar 

  23. Callac, P., Desmerger, C., Kerrigan, R.W., and Imbernon, M., Conservation of Genetic Linkage with Map Expansion in Distantly Related Crosses of Agaricus bisporus, FEMS Microbiol. Lett., 1997, vol. 146, pp. 235–240.

    CAS  PubMed  Google Scholar 

  24. Mazheika, I.S. and Kolomiets, O.L., A Method for Preparation of Synaptonemal Complexes of Meiotic Chromosomes from Basidial Protplasts of the White Button Mushroom Agaricus bisporus (Lange) Imbach, Rus. J. Genet., 2003, vol. 39, no. 3, pp. 283–287.

    Article  CAS  Google Scholar 

  25. Seitz, L.C., Tang, K., Cummings, W.J., and Zolan, M.E., The rad9 Gene of Coprinus cinereus Encodes a Proline-Rich Protein Required for Meiotic Chromosome Condensation and Synapsis, Genetics, 1996, vol. 142, pp. 1105–1117.

    CAS  PubMed  Google Scholar 

  26. Kües, U., Life History and Developmental Processes in the Basidiomycete Coprinus cinereus, Microbiol. Mol. Biol., 2000, vol. 64, pp. 316–353.

    Google Scholar 

  27. Callac, P., Hocquart, S., Imbernon, M., et al., Bsn-t Alleles from French Field Strains of Agaricus bisporus, Appl. Environ. Microbiol., 1998, vol. 64, pp. 2105–2110.

    CAS  PubMed  Google Scholar 

  28. Takami, K., Matsuda, S., Sono, A., and Sakaguchi, K., A Meiotic DNA Polymerase from a Mushroom Agaricus bisporus, Biochem. J., 1994, vol. 299, pp. 335–340.

    CAS  PubMed  Google Scholar 

  29. Bostok, K. and Samner, E., Khromosoma eukarioticheskoi kletki (Chromosome of the Eukaryotic Cell), Moscow: Mir, 1981.

    Google Scholar 

  30. Royer, J.C., Hintz, W.E., Kerrigan, R.W., and Horgen, P.A., Electrophoretic Karyotype Analysis of the Button Mushroom, Agaricus bisporus, Genome, 1992, vol. 35, pp. 694–698.

    Google Scholar 

  31. Thielke, C., Meiotic Divisions in the Basidium, Basidium and Basidiocarp, Wells, K. and Wells, E.K., Eds., New York: Springer-Verlag, 1982, pp. 75–91.

    Google Scholar 

  32. Lu, B.C., Gallo, N., and Kües, U., White-Cap Mutants and Meiotic Apoptosis in the Basidiomycete Coprinus cinereus, Fungal Genet. Biol., 2003, vol. 39, pp. 82–93.

    Article  CAS  PubMed  Google Scholar 

  33. Fletcher, H.L., A Search for Synaptonemal Complexes in Ustilago maydis, J. Cell Sci., 1981, vol. 50, pp. 171–180.

    CAS  PubMed  Google Scholar 

  34. Saksena, K.N., Marino, R., Haller, M.N., and Lemke, P.A., Study on Development of Agaricus bisporus by Fluorescent Microscopy and Scanning Electron Microscopy, J. Bacteriol., 1976, vol. 126, pp. 417–428.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Mycology and Algology, Moscow State University, Moscow, 119899, Russia

    I. S. Mazheika & Yu. T. Dyakov

  2. Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 119991, Russia

    I. S. Mazheika, O. L. Kolomiets & Yu. F. Bogdanov

Authors
  1. I. S. Mazheika
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  2. O. L. Kolomiets
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  3. Yu. T. Dyakov
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  4. Yu. F. Bogdanov
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Original Russian Text © I.S. Mazheika, O.L. Kolomiets, Yu.T. Dyakov, Yu.F. Bogdanov, 2006, published in Genetika, 2006, Vol. 42, No. 3, pp. 361–368.

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Mazheika, I.S., Kolomiets, O.L., Dyakov, Y.T. et al. Abnormal meiosis in bisporic strains of white button mushroom Agaricus bisporus (Lange) imbach. Russ J Genet 42, 279–285 (2006). https://doi.org/10.1134/S1022795406030070

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  • DOI: https://doi.org/10.1134/S1022795406030070

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