Skip to main content
SpringerLink
Log in

A Trans-Activator on the Drosophila Y Chromosome Regulates Gene Expression in the Male Germ Line

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The Ychromosome of Drosophila melanogasteraccounts for approximately 13% of a normal male genome and is entirely heterochromatic. It carries six genes required exclusively for spermatogenesis. Here we report a novel activity of the Ychromosome that regulates gene expression in primary spermatocytes. By examining the expression of a reporter gene in X/Yand X/0males, we show that a specific region of the Ylong arm carries a trans-activator that regulates transcription in spermatogenesis. In the absence of the Ytrans-activator, the level of the reporter expression is greatly reduced in primary spermatocytes and the expression pattern is restricted to young primary spermatocytes. Further analysis shows that the Ytrans-activator is dispersed in the h1-h10 region on the Ylong arm and is functionally redundant, indicating involvement of the repetitive sequences on the Ychromosome. In addition, the Ytrans-activator appears to act in a tissue-specific manner, functioning only in the male germ line. We propose that the Ytrans-activator plays an important role in regulating gene expression during spermatogenesis.

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

  • Appels, R. & W.J. Peacock, 1978. The arrangement and evolution of highly repeated (satellite) DNA sequences with special reference to Drosophila. Int. Rev. Cytol. (Suppl.) 8: 69–126.

    CAS  Google Scholar 

  • Bonaccorsi, S. & A. Lohe, 1991. Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationship between satellite sequences and fertility factors. Genetics 129: 177–189.

    PubMed  CAS  Google Scholar 

  • Bonaccorsi, S., M. Gatti, C. Pisano & A. Lohe, 1990. Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma 99: 260–266.

    Article  PubMed  CAS  Google Scholar 

  • Bonaccorsi, S., C. Pisano, F. Puoti & M. Gatti, 1988. Y chromosome loops in Drosophila melanogaster. Genetics 120: 1015– 1034.

  • Bourgouin, C., S.E. Lundgren & J.B. Thomas, 1992. Apterous is a DrosophilaLIM domain gene required for the development of a subset of embryonic muscles. Neuron 9: 549–561.

    Article  PubMed  CAS  Google Scholar 

  • Casadaban, M.J., A. Martinez-Arias, S.K. Shapira & J. Chou, 1983. Beta-galactosidase gene fusions for analyzing gene expression in Escherichia coliand yeast. Methods Enzymol. 100: 293–308.

    Article  PubMed  CAS  Google Scholar 

  • Castrillon, D., P. Gonczy, S. Alexander, R. Rawson, C. Eberhart, S. Viswanathan, S. DiNardo & S.A. Wasserman, 1993. Towards a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135: 489–505.

    PubMed  CAS  Google Scholar 

  • Castrillon, D.H. & S.A. Wasserman, 1994. Diaphanous is required for cytokinesis in Drosophilaand shares domains of similarity with the products of the limb deformity gene. Development 120: 3367–3377.

    PubMed  CAS  Google Scholar 

  • Clemson, C., J. McNeil, H. Willard & J. Lawrence, 1996. Xist RNA paints the inactive X chromosome at interphase: evidence for novel RNA involved in nuclear/chromosome structure. J. Cell Biol. 132: 259–275.

    Article  PubMed  CAS  Google Scholar 

  • Csink, A.K. & S. Henikoff, 1998. Something from nothing: the evolution and utility of satellite repeats. Trends Genet. 14: 200-204.

    Article  PubMed  CAS  Google Scholar 

  • Dietzel, S., H. Niemann, B. Bruckner, C. Maurange & R. Paro, 1999. The nuclear distribution of Polycomb during Drosophila melanogasterdevelopment shown with a GFP fusion protein. Chromosoma 108: 83–94.

    Article  PubMed  CAS  Google Scholar 

  • Dimitri, P. & C. Pisano, 1989. Position effect variegation in Drosophila melanogaster: relationship between suppression effect and the amount of Y chromosome. Genetics 122: 793–800.

    PubMed  CAS  Google Scholar 

  • Elgin, S.C.R. 1996. Heterochromatin and gene regulation in Drosophila. Curr. Opin. Genet. Dev. 6: 193–202.

    Article  PubMed  CAS  Google Scholar 

  • Fuller, M., 1993. Spermatogenesis, pp. 71–147 in The Development of Drosophila melanogaster, edited by M. Bate & A. Martinez. Cold Spring Harbor Laboratory Press.

  • Gatti, M. & S. Pimpinelli, 1983. Cytological and genetic analysis of the Y chromosome of Drosophila melanogaster. I. Organization of the fertility factors. Chromosoma 88: 349–373.

    Article  Google Scholar 

  • Gatti, M. & S. Pimpinelli, 1992. Functional elements in Drosophila melanogasterheterochromatin. Ann. Rev. Genet. 26: 239–275.

    Article  PubMed  CAS  Google Scholar 

  • Gepner, J. & T. Hays, 1993. A fertility region on the Y chromosome of D. melanogasterencodes a dynein microtubule motor. Proc. Natl. Acad. Sci. USA 90: 11132-11136.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein, L., R. Hardy & D.L. Lindsley, 1982. Structural genes on the Y chromosome of D. melanogaster. Proc. Natl. Acad. Sci. USA 79: 7405–7409.

    Article  PubMed  CAS  Google Scholar 

  • Hackstein, J.H.P., 1987. Spermatogenesis in Drosophila, pp. 63–116 in Spermatogenesis: Genetic Aspects. Results and Problems in Cell Differentiation, Vol. 15, edited W. Hennig. Springer Verlag, Berlin, Heidelberg, New York.

    Google Scholar 

  • Hardy, R.W., K.T. Tokuyasu & D.L. Lindsley, 1981. Analysis of spermatogenesis in Drosophila melanogasterbearing deletions for Y-chromosome fertility genes. Chromosoma 88: 593–617.

    Article  Google Scholar 

  • Hardy, R.W., D.L. Lindsley, K.J. Livak, B. Lewis, A.L. Sivertsen, G.L. Joslyn, J. Edwards & S. Bonaccorsi, 1984. Cytogenetic analysis of a segment of the Y chromosome of Drosophila melanogaster. Genetics 107: 591–610.

    PubMed  CAS  Google Scholar 

  • Hazelrigg, T., P. Fornili & T. Kaufman, 1982. A cytogenetic analysis of X-ray induced male sterile on the Y chromosome of Drosophila melanogaster. Chromosoma 87: 535–559.

    Article  Google Scholar 

  • Heatwole, V.M. & S.R. Haynes, 1996. Association of RB97D, an RRM protein required for male fertility, with a Y chromosome lampbrush loop in Drosophilaspermatocytes. Chromosoma 105: 285–292.

    Article  PubMed  CAS  Google Scholar 

  • Karpen, G.H. & A.C. Spradling, 1992. Analysis of subtelomeric heterochromatin in a Drosophilaminichromosome by single P element insertional mutagenesis. Genetics 132: 737–753.

    PubMed  CAS  Google Scholar 

  • Karsch-Mizrachi, I. & S.R. Haynes, 1993. The Rb97D gene encodes a potential RNA-binding protein required for spermatogenesis in Drosophila. Nucleic Acids Res. 9: 2229–2235.

    Google Scholar 

  • Kassis, J.A., 1990. Spatial and temporal control elements of the Drosophilaengrailed gene. Genes Dev. 4: 433–443.

    PubMed  CAS  Google Scholar 

  • Kennison, J.A., 1981. The genetic & cytological organization of the Y chromosome of Drosophila melanogaster. Genetics 98: 529–548.

    PubMed  Google Scholar 

  • Lin, T., S. Viswanathan, C. Wood, P. Wilson, N. Wolf & M. Fuller, 1996. Coordinate developmental control of the meiotic cell cycle and spermatid differentiation in Drosophilamales. Development 122: 1331–1341.

    PubMed  CAS  Google Scholar 

  • Lindsley, D. & K.T. Tokuyasu, 1980. Spermatogenesis, pp. 225–294 in Genetics and Biology in Drosophila, 2nd edition, edited M. Ashburner & T. Wright. Academic Press, New York.

    Google Scholar 

  • Lohe, A., A. Hilliker & P. Roberts, 1993. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134: 1149–1174.

    PubMed  CAS  Google Scholar 

  • Marsh, J.L. & E. Wieschaus, 1978. Is sex determination in germ line and soma controlled by separate genetic mechanisms? Nature 272: 249–251.

    Article  PubMed  CAS  Google Scholar 

  • Meller, V.H., K.H. Wu, G. Roman, M.I. Kuroda & R.L. Davis, 1997. roX1 RNA paints the X chromosome of male Drosophilaand is regulated by the dosage compensation system. Cell 88:445–457.

    Article  PubMed  CAS  Google Scholar 

  • Mlodzik, M. & Y. Hiromi, 1992. The enhancer trap method in Drosophila: its application to neurobiology, pp. 397–414 in Gene Expression in Neural Tissues (Methods in Neuroscience 9), edited P.M. Cann. Academic Press, Orlando, Florida.

    Google Scholar 

  • Montell, D.J., P. Rorth & A.C. Spradling, 1992. slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes a DrosophilaC/EBP homolog. Cell 71: 51–62.

    Article  PubMed  CAS  Google Scholar 

  • Pak, D.T., M. Pflumm, I. Chesnokov, D.W. Huang, R. Kellum, J. Marr, P. Romanowski & M.R. Botchan, 1998. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91: 311–323.

    Article  Google Scholar 

  • Pimpinelli, S., M. Berloco, L. Fanti, P. Dimitri, S. Bonaccorsi, E. Marchetti, R. Caizzi, C. Caggese & M. Gatti, 1995. Transposable elements are stable structural components of Drosophila melanogasterheterochromatin. Proc. Natl. Acad. Sci. USA 92: 3804–3808.

    Article  PubMed  CAS  Google Scholar 

  • Platero, J., A. Csink, A. Quintanilla & S. Henikoff, 1998. Changes in chromosomal localization of heterochromatin-binding proteins during the cell cycle in Drosophila. J. Cell Biol. 140: 1297–1306.

    Article  PubMed  CAS  Google Scholar 

  • Santel, A., Winhauer, T., Blumer, N. & R. Renkawitz-Pohl, 1997. The Drosophila don juan (dj)gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev. 64: 19–30.

    Article  PubMed  CAS  Google Scholar 

  • Spofford, J.B., 1976. Position-effect variegation in Drosophila, pp. 955–1018 in The Genetics and Biology of Drosophila, Vol. 1c, edited by M. Ashburner & E. Novitiski. Academic Press, New York.

    Google Scholar 

  • Tautz, D. & C. Pfeifle, 1989. A non-radioactive in situhybridization method for the localization of specific RNAs in Drosophilaembryos reveals translational control of the segmentation gene hunchback. Chromosoma 98: 81–85.

    Article  PubMed  CAS  Google Scholar 

  • White-Cooper, H., M. Schäfer, L. Alphey & M. Fuller, 1998. Transcriptional and post-transcriptional control mechanisms coordinate the onset of spermatid differentiation with meiosis I in Drosophila. Development 125: 125–134.

    PubMed  CAS  Google Scholar 

  • Wallrath, L., 1998. Unfolding the mysteries of heterochromatin. Curr. Opin. Genet. Dev. 8: 147–153.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, P. & A.C. Spradling, 1994. Insertional mutagenesis of Drosophila heterochromatinwith single P elements. Proc. Natl. Acad. Sci. USA 91: 3539–3542.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, P. & R.L. Stankiewicz, 1998. Y-linked male sterile mutations induced by P element in Drosophila melanogaster. Genetics 150: 735–744.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular and Cell Biology, U-2131, University of Connecticut, 354 Mansfield Road, Storrs, CT, 06269-2131, USA

    Ping Zhang

  2. Department of Molecular and Cell Biology, U-2131, University of Connecticut, 354 Mansfield Road, Storrs, CT, 06269-2131, USA

    Benjamin Timakov, Rebecca L. Stankiewicz & Ismail Y. Turgut

Authors
  1. Ping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benjamin Timakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rebecca L. Stankiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ismail Y. Turgut
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, P., Timakov, B., Stankiewicz, R.L. et al. A Trans-Activator on the Drosophila Y Chromosome Regulates Gene Expression in the Male Germ Line. Genetica 109, 141–150 (2000). https://doi.org/10.1023/A:1026504721067

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026504721067

Search

Navigation