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Molecular Evolution of Tandemly Repeated Heterochromatic Gene Clusters Involving a Switch of Their Function in the Genome of Drosophila melanogaster

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Abstract

Molecular evolution and divergence of paralogous tandem heterochromatic repeats Stellate and Su(Ste) located on the X and Y chromosomes, respectively, are discussed. These repeats appear to emerge as a result of amplification of a unique autosomal euchromatic gene encoding the regulatory β-subunit of the CK2 protein kinase. The autosomal gene and the clusters of heterochromatic repeats are transcribed in testes. A high level of the Stellate expression leads to partial male sterility and abnormal meiosis. The Stellate expression and its adverse effects are suppressed by homologous Su(Ste) repeats. In genome evolution, the open reading frames (ORF) of Stellate and Su(Ste) putative ancestor were maintained by translational selection. Then the coding Su(Ste) function has been damaged and switched to a new one resulting in antisense Su(Ste) transcription and silencing of theStellategenes. Symmetrical (sense and antisense) Su(Ste) transcription causes the formation of a double-strand RNA, which by interference (selective elimination of the homologous gene expression) suppresses the Stellate genes. The biological significance and the driving forces of evolution of the species-specific balanced interaction of Stellateand Su(Ste) repeats remain mysterious.

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REFERENCES

  1. Liao, D., Molecular Evolution '99: Concerted Evolution: Molecular Mechanism and Biological Implications, Am. J. Hum. Genet., 1999, vol. 64, pp. 24-30.

    Google Scholar 

  2. Hardy, R.W., Lindsley, D.L., Livak, K.J., et al., Cytogenetic Analysis of a Segment of the Y Chromosome of Drosophila melanogaster, Genetics, 1984, vol. 107, pp. 591-610.

    Google Scholar 

  3. Livak, K.J., Organization and Mapping of a Sequence of Drosophila melanogaster X and Y Chromosomes That Is Transcribed during Spermatogenesis, Genetics, 1984, vol. 107, pp. 611-634.

    Google Scholar 

  4. Livak, K.J., Detailed Structure of the Drosophila melanogaster Stellate Genes and Their Transcripts, Genetics, 1990, vol. 124, pp. 303-316.

    Google Scholar 

  5. Bozzetti, M., Massari, S., Finelli, P., et al., The Ste Locus, a Component of the Parasitic Cry-Ste System of Drosophila melanogaster, Encodes a Protein That Forms Crystals in Primary Spermatocytes and Mimics Properties of the β Subunit of Casein Kinase 2, Proc. Natl. Acad. Sci. USA, 1995, vol. 92, pp. 6067-6071.

    Google Scholar 

  6. Hurst, L.D., Further Evidence Consistent with Stellate's Involvement in Meiotic Drive, Genetics, 1996, vol. 142, pp. 641-643.

    Google Scholar 

  7. Hurst, L.D. and Smith, N.G.C., The Evolution of Concerted Evolution, Proc. R. Soc. London, B, 1998, vol. 265, pp. 121-127.

    Google Scholar 

  8. Kalmykova, A.I., Dobritsa, A.A., and Gvozdev, V.A., The Su(Ste) Repeat in the Y Chromosome and βCK2tes Gene Encode Predicted Isoforms of Regulatory β-Subunit of Protein Kinase CK2 in Drosophila melanogaster, FEBS Lett., 1997, vol. 416, pp. 164-166.

    Google Scholar 

  9. Palumbo, G., Berloco, M., Fanti, L., et al., Interaction Systems between Heterochromatin and Euchromatin in Drosophila melanogaster, Genetica (The Hague), 1994, vol. 94, pp. 267-274.

    Google Scholar 

  10. Shevelyov, Y., Copies of a Stellate Gene Variant Are Located in the X Heterochromatin of Drosophila melanogaster and Are Probably Expressed, Genetics, 1992, vol. 132, pp. 1033-1037.

    Google Scholar 

  11. Tulin, A.V., Kogan, G.L., Filipp, D., et al., Heterochromatic Stellate Gene Cluster in Drosophila melanogaster: Structure and Molecular Evolution, Genetics, 1997, vol. 146, pp. 253-262.

    Google Scholar 

  12. Zhimulev, I.F., Polytene Chromosomes, Heterochromatin and Position Effect Variegation, Adv. Genet., 1998, vol. 37, pp. 1-566.

    Google Scholar 

  13. Kalmykova, A.I., Shevelyov, Y.Y., Dobritsa, A.A., and Gvozdev, V.A., Acquisition and Amplification of a Testis-Expressed Autosomal Gene, SSL, by the Drosophila Y Chromosome, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 6927-6302.

    Google Scholar 

  14. Charlesworth, B., The Evolution of Chromosomal Sex Determination and Dosage Compensation, Curr. Biol., 1996, vol. 6, pp. 149-162.

    Google Scholar 

  15. Aravin, A.A., Naumova, N.M., Tulin, A.V., et al., Double-Stranded RNA-Mediated Silencing of Genomic Tandem Repeats and Transposable Elements in the D. melanogaster Germline, Curr. Biol., 2001, vol. 11, pp. 1017-1027.

    Google Scholar 

  16. Sharp, P.A., RNA Interference-2001, Genes. Dev., 2001, vol. 15, pp. 485-490.

    Google Scholar 

  17. Fire, A., Xu, S., Montgomery, M.K., et al., Potent and Specific Genetic Interference by Double-Stranded RNA in Caenorhabditis elegans, Nature, 1998, vol. 391, pp. 806-811.

    Google Scholar 

  18. Saxena, A., Carney, M., Bruley, M., and Glover, C.V.C., Characterization of Genes Encoding the α and β Subunits of Drosophila Casein Kinase II, Genetics, 1989, vol. 122, p. S25.

    Google Scholar 

  19. Balakireva, M.D., Shevelyov, Yu.Ya., Nurminsky, D.I., et al., Structural Organization and Diversification of Y-Linked Sequences Comprising Su(Ste) Genes in Drosophila melanogaster, Nucleic Acids Res., 1992, vol. 20, pp. 3731-3736.

    Google Scholar 

  20. Kalmykova, A.I., Dobritsa, A.A., and Gvozdev, V.A., Su(Ste) Diverged Tandem Repeats in the Y Chromosome of Drosophila melanogaster Are Transcribed and Variously Processed, Genetics, 1998, vol. 148, pp. 243-249.

    Google Scholar 

  21. Kogan, G.L., Epstein, V.N., Aravin, A.A., and Gvozdev, V.A., Molecular Evolution of Two Paralogous Tandemly Repeated Heterochromatic Gene Clusters Linked to the X and Y Chromosomes of Drosophila melanogaster, Mol. Biol. Evol., 2000, vol. 17, pp. 697-702.

    Google Scholar 

  22. Chantalat, L., Leroy, D., Filhol, O., et al., Crystal Structure of the Human Protein Kinase CK2 Regulatory Subunit Reveals Its Zinc Finger-Mediated Dimerization, EMBO J., 1999, vol. 18, pp. 2930-2940.

    Google Scholar 

  23. Sharp, P.M. and Matassi, G., Codon Usage and Genome Evolution, Curr. Opin. Genet. Dev., 1994, vol. 4, pp. 851-860.

    Google Scholar 

  24. Akashi, H., Codon Bias Evolution in Drosophila: Population Genetics of Mutation-Selection Drift, Gene, 1997, vol. 205, pp. 269-278.

    Google Scholar 

  25. Powell, J.R. and Moriyama, E.N., Evolution of Codon Usage Bias in Drosophila, Proc. Natl. Acad. Sci. USA, 1997, vol. 94, pp. 7784-7790.

    Google Scholar 

  26. McKee, B. and Satter, M.T., Structure of the Y-Chromosomal Su(Ste) Locus in Drosophila melanogaster and Evidence for Localized Recombination among Repeats, Genetics, 1996, vol. 142, pp. 149-161.

    Google Scholar 

  27. Palumbo, G., Bonaccorsi, S., Robbins, L.G., and Pimpinelli, S., Genetic Analysis of Stellate Elements of Drosophila melanogaster, Genetics, 1994, vol. 138, pp. 1181-1197.

    Google Scholar 

  28. Robbinns, L. and Belloni, M., Who Causes Meiotic Drive—Ste + or cry -?, 17th Eur. Drosophila Res. Conf., 2001, Edinburgh, 2001, p. 39.

  29. Russo, C.A.M., Takezaki, N., and Nei, M., Molecular Phylogeny and Divergence Times of Drosophilid Species, Mol. Biol. Evol., 1995, vol. 12, pp. 391-404.

    Google Scholar 

  30. Danilevskaya, O.N., Kurenova, E.V., Pavlova, M.N., et al., He-T Family DNA Sequences in the Y Chromosome of Drosophila melanogaster Share Homology with the X-Linked Stellate Genes, Chromosoma, 1991, vol. 100, pp. 118-124.

    Google Scholar 

  31. Tuschl, T., Zamore, P.D., Lehmann, R., et al., Targeted mRNA Degradation by Double-Stranded RNA in Vitro, Genes Dev., 1999, vol. 13, pp. 3191-3197.

    Google Scholar 

  32. Tabara, H., Sarkissian, M., Kelly, W.G., et al., The rde-1 Gene, RNA Interference, and Transposon Silencing in C. elegans, Cell (Cambridge, Mass.), 1999, vol. 99, pp. 123-132.

    Google Scholar 

  33. Schmidt, A., Palumbo, G., Bozetti, M.P., et al., Genetic and Molecular Characterization of Sting, a Gene Involved in Crystal Formation and Meiotic Drive in the Male Germ Line of Drosophila melanogaster, Genetics, 1989, vol. 151, pp. 749-760.

    Google Scholar 

  34. Ketting, R.F., Haverkamp, T.H., van Luenen, H.G., and Plasterk, R.H., Mut-7 of C. elegans, Required for Transposon Silencing and RNA Interference, Is a Homolog of Werner Syndrome Helicase and RNase D, Cell (Cambridge, Mass.), 1999, vol. 99, pp. 133-141.

    Google Scholar 

  35. Knight, S.W. and Bass, B.L., A Role for the RNase III Enzyme DCRI in RNA Interference and Germ Line Development in C. elegans, Science, 2001, vol. 293, pp. 2269-2271.

    Google Scholar 

  36. Hutvagner, G., McLachlan, J., Pasquinelli, A.E., et al., A Cellular Function for the RNA-Interference Enzyme Dicer in the Maturation of the let-7 Small Temporal RNA, Science, 2001, vol. 293, pp. 834-838.

    Google Scholar 

  37. Thompson-Steward, D., Karpen, G.H., and Spradling, A.C., A Transposable Element Can Drive the Concerted Evolution of Tandemly Repetitious DNA, Proc. Natl. Acad. Sci. USA, 1994, vol. 91, pp. 9042-9046.

    Google Scholar 

  38. Spradling, A.C., Transposable Elements and the Evolution of Heterochromatin, in Molecular Evolution of Physiological Process, Rockefeller Univ. Press, 1994, pp. 76-83.

  39. Williams, S.M., Furiner, G.R., Fuog, E., and Strobeck, C., Evolution of Ribosomal DNA Spacers of Drosophila melanogaster: Different Patterns of Variation on X and Y Chromosomes, Genetics, 1987, vol. 116, pp. 225-232.

    Google Scholar 

  40. Parniske, M., Hammond-Kosack, K.E., Goldstein, C., et al., Novel Disease Resistance Specificities Result from Sequence Exchange between Tandemly Repeated Genes at the Cf-4/9 Locus of Tomato, Cell (Cambridge, Mass.), 1997, vol. 91, pp. 821-832.

    Google Scholar 

  41. Nassif, N. and Engels, W., DNA Homology Requirements for Mitotic Gap Repair in Drosophila, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 1262-1266.

    Google Scholar 

  42. Lahn, B.T., Pearson, N.M., and Jegalian, K., The Human Y Chromosome in the Light of Evolution, Nat. Rev. Genet., 2001, vol. 2, pp. 207-216.

    Google Scholar 

  43. Lahn, B.T. and Page, D.C., Four Evolutionary Strata on the Human X Chromosome, Science, 1999, vol. 286, pp. 964-967.

    Google Scholar 

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  1. Institute of Molecular Genetics, Russian Academy of Sciences, Moscow, 123182, Russia

    G. L. Kogan & V. A. Gvozdev

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  1. G. L. Kogan
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Kogan, G.L., Gvozdev, V.A. Molecular Evolution of Tandemly Repeated Heterochromatic Gene Clusters Involving a Switch of Their Function in the Genome of Drosophila melanogaster. Russian Journal of Genetics 38, 586–593 (2002). https://doi.org/10.1023/A:1016075414124

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