Russian Journal of Genetics

, Volume 46, Issue 9, pp 1058–1061

Molecular genome organization in ciliates



The review summarizes modern views on to the structure and differentiation of the nuclear apparatus in ciliates. The genetic system of ciliates (type Ciliophora) includes two types of nuclei: germinal micronucleus (MIC) and somatic macronucleus (MAC). The MAC development is associated with the rearrangement of the MIC genome, which includes chromosome fragmentation and chromatin diminution. The loss of DNA constitutes from 10–15% (Tetrahymena termophila) to 95–98% of the genome in spirotrichs (Stylonychia, Oxytricha, and Euplotes). Analysis of molecular mechanisms underlying nuclear dualism in ciliates promoted radical revision of the concept on the interactions and roles of MAC and MIC. The micronucleus, as an inactive element, is an ideal field for the invasion and further expansion of mobile genetic elements. Chromatin diminution plays the purifying role, restoring the native genome structure. The process of recognition of “genetic garbage” to be eliminated has many features in common with the siRNA-mediated heterochromatization. The presence of this mechanism in very early radiated eukaryotic lineages (Opistokonta and Chromalveolata), indicates that it arose at the earliest stages of the eukaryotic evolution, probably, as a mechanism promoting genome integrity and stability.


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  1. 1.
    Raikov, I.B., The Protozoan Nucleus, Wien: Springer, 1982.Google Scholar
  2. 2.
    Jahn, C.L. and Klobutcher, L.A., Genome Remodeling in Ciliated Protozoa, Annu. Rev. Microbiol., 2002, vol. 56, pp. 489–520.CrossRefPubMedGoogle Scholar
  3. 3.
    Gratias, A. and Betermier, M., Developmentally Programmed Excision of Internal DNA Sequences in Paramecium aurelia, Biochimie, 2001, vol. 83, pp. 1009–1022.CrossRefPubMedGoogle Scholar
  4. 4.
    Austerberry, C.F. and Yao, M.C., Nucleotide Sequence Structure and Consistency of a Developmentally Regulated DNA Deletion in Tetrahymena thermophila, Mol. Cell. Biol., 1987, vol. 7, pp. 435–443.PubMedGoogle Scholar
  5. 5.
    Coyne, R.S., Chalker, D.L., and Yao, M.C., Genome Downsizing during Ciliate Development: Nuclear Division of Labor through Chromosome Restructuring, Ann. Rev. Genet., 1996, vol. 30, pp. 557–578.CrossRefPubMedGoogle Scholar
  6. 6.
    Chalker, D.L. and Yao, M.C., Non-Mendelian, Heritable Blocks to DNA Rearrangement Are Induced by Loading the Somatic Nucleus of Tetrahymena thermophila with Germ Line-Limited DNA, Mol. Cell. Biol., 1996, vol. 16, pp. 3658–3667.PubMedGoogle Scholar
  7. 7.
    Yao, M.C., Yao, C.H., and Monks, B., The Controlling Sequence for Site-Specific Chromosome Breakage in Tetrahymena, Cell, 1990, vol. 63, pp. 763–772.CrossRefPubMedGoogle Scholar
  8. 8.
    Klobutcher, L.A., Gygax, S.E., Podoloff, J.D., et al., Conserved DNA Sequences Adjacent to Chromosome Fragmentation and Telomere Addition Sites in Euplotes crassus, Nucl. Acids Res., 1998, vol. 26, pp. 4230–4240.CrossRefPubMedGoogle Scholar
  9. 9.
    Le Mouë, A., Butler, A., Caron, F., et al., Developmentally Regulated Chromosome Fragmentation Linked to Imprecise Elimination of Repeated Sequences in Paramecia, Eukaryot. Cell, 2003, vol. 2, pp. 1076–1090.CrossRefGoogle Scholar
  10. 10.
    Katz, L.A., Evolution of Nuclear Dualism in Ciliates: A Reanalysis in Light of Recent Olecular Data, Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 1587–1592.PubMedGoogle Scholar
  11. 11.
    Rautian, M.S. and Potekhin, A.A., Electrokaryotypes of Macronuclei of Several Paramecium Species, Eukaryot. Microbiol., 2002, vol. 49, pp. 296–304.CrossRefGoogle Scholar
  12. 12.
    Klobutcher, L.A. and Herrick, G., Consensus Inverted Terminal Repeat Sequence of Paramecium IESs: Resemblance to Termini of Tc1-Related and Euplotes Tec Transposons, Nucl. Acids Res., 1995, vol. 23, pp. 2006–2013.CrossRefPubMedGoogle Scholar
  13. 13.
    Duharcourt, S., Butler, A., and Meyer, E., Epigenetic Self-Regulation of Developmental Excision of an Internal Eliminated Sequence in Paramecium tetraurelia, Genes Dev., 1995, vol. 9, pp. 2065–2077.CrossRefPubMedGoogle Scholar
  14. 14.
    Duharcourt, S., Keller, A.M., and Meyer, E., Homology Dependent Maternal Inhibition of Developmental Excision of Internal Eliminated Sequences in Paramecium tetraurelia, Mol. Cell. Biol., 1998, vol. 18, pp. 7075–7085.PubMedGoogle Scholar
  15. 15.
    Meyer, E. and Garnier, O., Non-Mendelian Inheritance and Homology-Dependent Effects in Ciliates, Adv. Genet., 2002, vol. 46, pp. 305–337.CrossRefPubMedGoogle Scholar
  16. 16.
    Sugai, T. and Hiwatashi, K., Cytologic and Autoradiographic Studies of the Micronucleus at Meiotic Prophase in Tetrahymena pyriformis, J. Protozool., 1974, vol. 21, pp. 542–548.PubMedGoogle Scholar
  17. 17.
    Martindale, D.W., Allis, C.D., and Bruns, P.J., RNA and Protein Synthesis during Meiotic Prophase in Tetrahymena thermophila, J. Protozool., 1985, vol. 32, pp. 644–649.PubMedGoogle Scholar
  18. 18.
    Chalker, D.L. and Yao, M.C., Nongenic, Bidirectional Transcription Precedes and May Promote Developmental DNA Deletion in Tetrahymena thermophila, Genes Dev., 2001, vol. 15, pp. 1287–1298.CrossRefPubMedGoogle Scholar
  19. 19.
    Garnier, O., Serrano, V., Duharcourt, S., et al., RNA-Mediated Programming of Developmental Genome Rearrangements in Paramecium tetraurelia, Mol. Cell. Biol., 2004, vol. 24, pp. 7370–7379.CrossRefPubMedGoogle Scholar
  20. 20.
    Mochizuki, K., Fine, N., Fujisawa, T., et al., Analysis of a piwi-Related Gene Implicates Small RNAs in Genome Rearrangement in Tetrahymena, Cell, 2002, vol. 110, pp. 689–699.CrossRefPubMedGoogle Scholar
  21. 21.
    Yao, M.C. and Chao, J., RNA-Guided DNA Deletion in Tetrahymena: An RNAi-Based Mechanism for Programmed Genome Rearrangements, Ann. Rev. Genet., 2005, vol. 39, pp. 537–559.CrossRefPubMedGoogle Scholar
  22. 22.
    Mochizuki, K. and Gorovsky, M.A., Small RNAs in Genome Rearrangement in Tetrahymena, Curr. Opin. Genet. Dev., 2004, vol. 14, pp. 181–187.CrossRefPubMedGoogle Scholar
  23. 23.
    Motamedi, M.R., Verdel, A., Colmenares, S.U., et al., Two RNAi Complexes, RITS and RDRC, Physically Interact and Localize to Noncoding Centromeric RNAs, Cell, 2004, vol. 119, pp. 789–802.CrossRefPubMedGoogle Scholar
  24. 24.
    Taverna, S.D., Coyne, R.S., and Allis, C.D., Methylation of Histone h3 at Lysine 9 Targets Programmed DNA Elimination in Tetrahymena, Cell, 2002, vol. 110, pp. 701–711.CrossRefPubMedGoogle Scholar
  25. 25.
    Liu, Y., Taverna, S.D., Muratore, T.L., et al., RNAi Dependent H3K27 Methylation Is Required for Heterochromatin Formation and DNA Elimination in Tetrahymena, Genes Dev., 2007, vol. 21, pp. 1530–1545.CrossRefPubMedGoogle Scholar
  26. 26.
    Aronica, L., Bednenko, J., Noto, T., et al., Study of an RNA Helicase Implicates Small RNA-Noncoding RNA Interactions in Programmed DNA Elimination in Tetrahymena, Genes Dev., 2008, vol. 22, pp. 2228–2241.CrossRefPubMedGoogle Scholar
  27. 27.
    Lepère, G., Be’termier, M., Meyer, E., et al., Maternal Noncoding Transcripts Antagonize the Targeting of DNA Elimination by scanRNAs in Paramecium tetraurelia, Genes Dev., 2008, vol. 22, pp. 1501–1512.CrossRefPubMedGoogle Scholar
  28. 28.
    Duharcourt, S., Lepère, G., and Meyer, E., Developmental Genome Rearrangements in Ciliates: A Natural Genomic Subtraction Mediated by Non-Coding Transcripts, Trends Genet., 2009, vol. 25, pp. 344–350.CrossRefPubMedGoogle Scholar
  29. 29.
    Malinsky, B.C., Restituito, S., Kapusta, D., et al., PiggyMac, a Domesticated piggyBac Transposase Involved in Programmed Genome Rearrangements in the Ciliate Paramecium Tetraurelia, Genes Dev., 2009, vol. 23, pp. 2478–2483.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  1. 1.Department of Invertebrate ZoologySt. Petersburg State UniversitySt. PetersburgRussia

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