Skip to main content
Log in

Chromosomally-Induced Meiotic Drive in Drosophila Males: Checkpoint or Fallout?

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

In male Drosophila melanogaster, anomalies in sex chromosome pairing at meiosis often lead to complete or partial sperm dysfunction. This observation has led to the suggestion that defects in either the efficiency or configuration of chromosome pairing at metaphase trigger a checkpoint mechanism that leads to the elimination of meiotic products. Here, we discuss this model in consideration of recent observations on the conservation of metaphase checkpoint components in male meiosis, and on the phenotype of new alleles of the male-specific meiotic mutant teflon. Based on these observations, we propose an alternative hypothesis for the cause of sperm dysfunction in cases of chromosomal sterility and drive. We suggest that disruption of the prophase compartmentalization of sex chromatin, rather than abnormal pairing at metaphase, may be the causative defect. Such disruption may occur as a result of perturbations in sex chromosome pairing, or by translocations involving autosomal and sex chromatin. We discuss how this hypothesis may account for previously described examples chromosomal causes of meiotic drive and sterility in Drosophila.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baker, B.S. & A.T.C. Carpenter, 1972. Genetic analysis of sex chromosomal meiotic mutants in Drosophila melanogaster. Genetics 71: 255–286.

    PubMed  CAS  Google Scholar 

  • Basu, J., E. Logarinho, Z. Li, B.C. Williams, C. Lopes, C. E. Sunkel & M.L. Goldberg, 1999. Mutations in the essential spindle checkpoint gene bub1 cause chromosome missegregation and fail to block apoptosis in Drosophila. J. Cell Biol. 146: 13–28.

    PubMed  CAS  Google Scholar 

  • Basu, J., S. Herrmann, H. Bousbaa, Z. Li, G.K. Chan, T.J. Yen, C.E. Sunkel & M.L. Goldberg, 1998. Localization of the Drosophilacheckpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod. Chromosoma 107: 376–385.

    Article  PubMed  CAS  Google Scholar 

  • Briscoe, A. Jr. & J.E. Tomkiel, 2000. Chromosomal position effects reveal different requirements for rDNA transcription and sex chromosome pairing in Drosophila melanogaster. Genetics 155: 1195–1211.

    PubMed  CAS  Google Scholar 

  • Cooper, K.W., 1950. Normal spermatogenesis in Drosophila, pp. 1–61 in The Biology of Drosophila, edited by M. Demerec. Wiley, New York.

    Google Scholar 

  • Cryderman, D.E., E.J. Morris, H. Biessman, S.C.R. Elgin & L.L. Wallrath, 1999. Silencing at Drosophilatelomeres: nuclear organization and chromatin structure play critical roles. EMBO J. 18: 3734–3735.

    Article  Google Scholar 

  • Dernburg, A., D. Daily, K. Yook, J. Corbin, J.W. Sedat & W. Sullivan, 1996. Selective loss of sperm bearing a compound chromosome in the Drosophilafemale. Genetics 143: 1629–1642.

    PubMed  CAS  Google Scholar 

  • Forejt, J., S. Gregorova & P. Goetz, 1981. XY pair associates with the synaptonemal complex of autosomal male-sterile translocations in pachytene spermatocytes of the mouse (Mus musculus). Chromosoma 82: 41–53.

    Article  PubMed  CAS  Google Scholar 

  • Hall, J. C., 1970. Non-independence of primary nondisjunction for the sex and fourth chromosomes in D. melanogaster. Drosophila Inf. Service 45: 160.

    Google Scholar 

  • Henikoff, S. & T.D. Dreesen, 1989. Trans-inactivation of the Drosophila browngene: evidence for transcriptional repression and somatic pairing dependence. Proc. Natl. Acad. Sci. USA 86: 6704–6708.

    Article  PubMed  CAS  Google Scholar 

  • Henikoff, S., J.M. Jackson & P. Talbert, 1995. Distance and pairing effects on the brown dominantheterochromatic element in Drosophila. Genetics 140: 1007–1017.

    PubMed  CAS  Google Scholar 

  • Li, R. & A.W. Murray, 1991. Feedback control of mitosis in budding yeast. Cell 66: 519–531.

    Article  PubMed  CAS  Google Scholar 

  • Li, X. & R.B. Nicklas, 1995. Mitotic forces control a cell-cycle checkpoint. Nature 373: 630–632.

    Article  PubMed  CAS  Google Scholar 

  • Lifschytz, E. & D.L. Lindsley, 1972. The role of X-chromosome inactivation during spermatogenesis. Proc. Natl. Acad. Sci. 69: 182–186.

    Article  PubMed  CAS  Google Scholar 

  • Lindsley, D.L. & L. Sandler, 1958. The meiotic behavior of grossly deleted X chromosomes in Drosophila melanogaster. Genetics 43: 547–563.

    PubMed  CAS  Google Scholar 

  • Lindsley, D.L. & K.T. Tokuyasu, 1980. Spermatogenesis, pp. 225–294 in The Genetics and Biology of Drosophila, edited by M. Ashburner and T.R.F. Wright. Academic Press, New York.

    Google Scholar 

  • Livak, K.J., 1990. Detailed structure of the Drosophila melanogasterStellate genes and their transcripts. Genetics 124: 303–316.

    PubMed  CAS  Google Scholar 

  • Lyttle, T., 1993. Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive. Trends Genet. 9: 205–210.

    Article  PubMed  CAS  Google Scholar 

  • Mason, J.M., 1976. Orientation disrupter (ord): a recombination defective and disjunction-defective meiotic mutant in Drosophila melanogaster. Genetics 84: 545–572.

    PubMed  CAS  Google Scholar 

  • McKee, B., 1987. X;4 translocations and meiotic drive in Drosophila melanogastermales: role of sex chromosome pairing. Genetics 116: 409–413.

    PubMed  Google Scholar 

  • McKee, B. & M.A. Handel, 1993. Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102: 71–80.

    Article  PubMed  CAS  Google Scholar 

  • McKee, B. & G.H. Karpen, 1990. Drosophilaribosomal RNA genes function as an X-Y pairing site during male meiosis. Cell 61: 61–72.

    Article  PubMed  CAS  Google Scholar 

  • McKee, B.D., 1984. Sex chromosome meiotic drive in Drosophila melanogastermales. Genetics 106: 403–422.

    PubMed  Google Scholar 

  • McKee, B.D., 1991. X-Y pairing, meiotic drive, and ribosomal DNA in Drosophila melanogastermales. Am. Nat. 137: 332–339.

    Article  Google Scholar 

  • McKee, B.D., L. Habera & J.A. Vrana, 1992. Evidence that intergenic spacer repeats of Drosophila melanogasterrRNA genes function as X-Y pairing sites in male meiosis, and a general model for achiasmatic pairing. Genetics 132: 529–544.

    PubMed  CAS  Google Scholar 

  • McKee, B.D. & D.L. Lindsley, 1987. Inseparability of Xheterochromatin functions responsible for X:Y pairing, meiotic drive, and male fertility in Drosophila melanogastermales. Genetics 116: 399–407.

    PubMed  Google Scholar 

  • McKee, B.D., S.E. Lumsden & S. Das, 1993. The distribution of male meiotic pairing sites on chromosome 2 of Drosophila melanogaster: meiotic pairing and segregation of 2-Y transpositions. Chromosoma 102: 180–194.

    Article  PubMed  CAS  Google Scholar 

  • McKee, B.D., K. Wilhelm, C. Merrill & X. Ren, 1998. Male sterility and meiotic drive associated with sex chromosome rearrangements in Drosophila: Role of X-Y pairing. Genetics 149: 143–155.

    PubMed  CAS  Google Scholar 

  • Merrill, C., L. Bayraktaroglu, A. Kusano & B. Ganetzky, 1999. Truncated RanGAP encoded by the Segregation Distorterlocus of Drosophila. Science 283: 1742–1745.

    Article  PubMed  CAS  Google Scholar 

  • Merrill, C.J., D. Chakravarti, L. Habera, S. Das, L. Eisenhour & B.D. McKee, 1992. Promoter-containing ribosomal DNA fragments function as X-Y meiotic pairing sites in D. melanogastermales. Dev. Genet. 13: 468–484.

    Article  PubMed  CAS  Google Scholar 

  • Moore, D.P., W.Y. Miyazaki, J.E. Tomkiel & T.L. Orr-Weaver, 1994. Double or nothing: A Drosophilamutation affecting chromosome segregation in both females and males. Genetics 136: 953–964.

    PubMed  CAS  Google Scholar 

  • Nicklas, R.B., 1997. How cells get the right chromosomes. Science 275: 632–637.

    Article  PubMed  CAS  Google Scholar 

  • Nicklas, R.B., S.C. Ward & G. Gorbsky, 1995. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J. Cell Biol. 130: 929–939.

    Article  PubMed  CAS  Google Scholar 

  • Novitski, E., D. Grace & C. Strommen, 1981. The entire compound autosomes of Drosophila melanogaster. Genetics 98: 257–273.

    PubMed  CAS  Google Scholar 

  • Novitski, E. & I. Sandler, 1957. Are all products of spermatogenesis regularly functional? Proc. Natl. Acad. Sci. USA 43: 318–324.

    Article  PubMed  CAS  Google Scholar 

  • Palumbo, G., S. Bonnacorsi, L. Robbins & S. Pimpinelli, 1994. Genetic analysis of Stellate elements of Drosophila melanogaster. Genetics 138: 1181–1197.

    PubMed  CAS  Google Scholar 

  • Peacock, W.J., G.L.G. Miklos & D.J. Goodchild, 1975. Sex chromosome meiotic drive systems in Drosophila melanogaster: I. Abnormal spermatid development in males with a heterochromatin deficient X chromosome (sc4sc8). Genetics 79: 613–634.

    PubMed  CAS  Google Scholar 

  • Pimpinelli, S. & P. Dimitri, 1989. Cytogenetic analysis of segregation distortion in Drosophila melanogaster: the cytological organization of the Responder (Rsp) locus. Genetics 121: 765–772.

    PubMed  CAS  Google Scholar 

  • Reider, C.L. & R.W. Cole, 1995. The checkpoint delaying anaphase in response to chromosome nonoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J. Cell Biol. 130: 941–948.

    Article  Google Scholar 

  • Richler, C., E. Uliel, A. Rosenman & J. Wahrman, 1989. Chromosomally derived sterile mice have a ‘fertile’ active XY chromatin conformation but no XY body. Chromosoma 97: 465–474.

    Article  PubMed  CAS  Google Scholar 

  • Robbins, L.G., 1999. Are unpaired chromosome spermicidal? A maximum likelihood analysis of segregation and meiotic drive in Drosophila melanogastermales deficient for ribosomal-DNA. Genetics 151: 251–262.

    PubMed  CAS  Google Scholar 

  • Rosenman, A., J. Wahrman, C. Richler, R. Voss, A. Persitz & B. Goldman, 1985. Meiotic associations between the XY chromosome and unpaired autosomal elements as a cause of human sterility. Cytogenet. Cell Genet 39: 19–29.

    Article  Google Scholar 

  • Sandler, L., D.L. Lindsley, B. Nicoletti & G. Trippa, 1968. Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics 60: 525–558.

    PubMed  CAS  Google Scholar 

  • Schmidt, A., G. Palumbo, M.P. Bozzetti, P. Tritto, S. Pimpinelli & U. Schafer, 1999. Genetic and molecular characterization of sting, a gene involved in crystal formation and meiotic drive in the male germ line of Drosophila melanogaster. Genetics 151: 749–760.

    PubMed  CAS  Google Scholar 

  • Skibbens, R.V. & P. Hieter, 1998. Kinetochores and the checkpoint mechanism that monitors for defects in the chromosome segregation machinery. Annu. Rev. Genet. 32: 307–337.

    Article  PubMed  CAS  Google Scholar 

  • Williams, B.C., M. Gatti & M.L. Goldberg, 1996. Bipolar spindle attachments affect redistributions of ZW10, a Drosophila centromere/kinetochore component required for accurate chromosome segregation. J. Cell Bio. 134: 1127–1140.

    Article  CAS  Google Scholar 

  • Wu, C.I., T.W. Lyttle, M.L. Wu & G.F. Lin, 1988. Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell 54: 179–189.

    Article  PubMed  CAS  Google Scholar 

  • Zimmering, S. & E.B. Bendbow, 1973. Meiotic behavior of asymmetric dyads in the male Drosophila. Genetics 73: 631–638.

    PubMed  CAS  Google Scholar 

  • Zimmering, S. & C.K. Wu, 1963. Radiation induced X-Y exchange and nondisjunction in spermatocytes of the immature testis of Drosophila. Genetics 48: 1619–1623.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tomkiel, J.E. Chromosomally-Induced Meiotic Drive in Drosophila Males: Checkpoint or Fallout?. Genetica 109, 95–103 (2000). https://doi.org/10.1023/A:1026544402411

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1026544402411

Navigation