Abstract
A recessive male sterile mutation (B2t8) that encodes a stable variant of the testis-specific beta 2-tubulin of Drosophila causes the assembly of aberrant microtubules both in vivo and in vitro. The B2t8 mutation appears to cause defects in the formation of interprotofilament bonds. In testes from homozygous mutant males, the most commonly observed aberrant structures were sheets of protofilaments curved to form an S in cross section rather than a normal, closed microtubule. These characteristic S-shaped structures appear in the meiotic spindle, in place of axonemes in differentiating spermatids, and in cytoplasmic microtubules, including those that lie next to the nucleus during nuclear elongation. Homozygous mutant males exhibit defects in chromosome movement and cytokinesis during meiosis, flagellar elongation, and nuclear shaping, indicating that the ability to form normal closed microtubules is required for each of these events. The presence of the aberrant microtubules in three architecturally different microtubule arrays demonstrates conclusively the multifunctional nature of the beta 2-tubulin gene product. Although the mutant beta 2-tubulin subunit causes assembly of aberrant microtubules in vitro and in homozygous males, in the presence of wild-type beta 2- tubulin in heterozygous males, the variant subunit coassembles with the wild-type subunit into functional sperm.
Full Text
The Full Text of this article is available as a PDF (4.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bordas J., Mandelkow E. M., Mandelkow E. Stages of tubulin assembly and disassembly studied by time-resolved synchrotron X-ray scattering. J Mol Biol. 1983 Feb 15;164(1):89–135. doi: 10.1016/0022-2836(83)90089-x. [DOI] [PubMed] [Google Scholar]
- Burton P. R., Himes R. H. Electron microscope studies of pH effects on assembly of tubulin free of associated proteins. Delineation of substructure by tannic acid staining. J Cell Biol. 1978 Apr;77(1):120–133. doi: 10.1083/jcb.77.1.120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Euteneuer U., McIntosh J. R. Polarity of midbody and phragmoplast microtubules. J Cell Biol. 1980 Nov;87(2 Pt 1):509–515. doi: 10.1083/jcb.87.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Euteneuer U., McIntosh J. R. Polarity of some motility-related microtubules. Proc Natl Acad Sci U S A. 1981 Jan;78(1):372–376. doi: 10.1073/pnas.78.1.372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hardy R. W. The influence of chromosome content on the size and shape of sperm heads in Drosophila melanogaster and the demonstration of chromosome loss during spermiogenesis. Genetics. 1975 Feb;79(2):231–264. doi: 10.1093/genetics/79.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heidemann S. R., McIntosh J. R. Visualization of the structural polarity of microtubules. Nature. 1980 Jul 31;286(5772):517–519. doi: 10.1038/286517a0. [DOI] [PubMed] [Google Scholar]
- Kalt M. R., Tandler B. A study of fixation of early amphibian embryos for electron microscopy. J Ultrastruct Res. 1971 Sep;36(5):633–645. doi: 10.1016/s0022-5320(71)90020-7. [DOI] [PubMed] [Google Scholar]
- Kemphues K. J., Kaufman T. C., Raff R. A., Raff E. C. The testis-specific beta-tubulin subunit in Drosophila melanogaster has multiple functions in spermatogenesis. Cell. 1982 Dec;31(3 Pt 2):655–670. doi: 10.1016/0092-8674(82)90321-x. [DOI] [PubMed] [Google Scholar]
- Kemphues K. J., Raff E. C., Kaufman T. C. Genetic analysis of B2t, the structural gene for a testis-specific beta-tubulin subunit in Drosophila melanogaster. Genetics. 1983 Oct;105(2):345–356. doi: 10.1093/genetics/105.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kemphues K. J., Raff E. C., Raff R. A., Kaufman T. C. Mutation in a testis-specific beta-tubulin in Drosophila: analysis of its effects on meiosis and map location of the gene. Cell. 1980 Sep;21(2):445–451. doi: 10.1016/0092-8674(80)90481-x. [DOI] [PubMed] [Google Scholar]
- Kemphues K. J., Raff R. A., Kaufman T. C., Raff E. C. Mutation in a structural gene for a beta-tubulin specific to testis in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3991–3995. doi: 10.1073/pnas.76.8.3991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kiefer B. I. Development, organization, and degeneration of the Drosophila sperm flagellum. J Cell Sci. 1970 Jan;6(1):177–194. doi: 10.1242/jcs.6.1.177. [DOI] [PubMed] [Google Scholar]
- Kirschner M. W., Honig L. S., Williams R. C. Quantitative electron microscopy of microtubule assembly in vitro. J Mol Biol. 1975 Dec 5;99(2):263–276. doi: 10.1016/s0022-2836(75)80144-6. [DOI] [PubMed] [Google Scholar]
- Mahowald A. P., Caulton J. H., Gehring W. J. Ultrastructural studies of oocytes and embryos derived from females flies carrying the grandchildless mutation in Drosophila subobscura. Dev Biol. 1979 Mar;69(1):118–132. doi: 10.1016/0012-1606(79)90279-3. [DOI] [PubMed] [Google Scholar]
- Mandelkow E. M., Herrmann M., Rühl U. Tubulin domains probed by limited proteolysis and subunit-specific antibodies. J Mol Biol. 1985 Sep 20;185(2):311–327. doi: 10.1016/0022-2836(85)90406-1. [DOI] [PubMed] [Google Scholar]
- Mandelkow E. M., Mandelkow E. Junctions between microtubule walls. J Mol Biol. 1979 Mar 25;129(1):135–148. doi: 10.1016/0022-2836(79)90064-0. [DOI] [PubMed] [Google Scholar]
- McIntosh J. R., Euteneuer U. Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol. 1984 Feb;98(2):525–533. doi: 10.1083/jcb.98.2.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rappaport R. Establishment and organization of the cleavage mechanism. Soc Gen Physiol Ser. 1975;30:287–304. [PubMed] [Google Scholar]
- Tokuyasu K. T. Dynamics of spermiogenesis in Drosophila melanogaster. 3. Relation between axoneme and mitochondrial derivatives. Exp Cell Res. 1974 Mar 15;84(1):239–250. doi: 10.1016/0014-4827(74)90402-9. [DOI] [PubMed] [Google Scholar]
- Tokuyasu K. T. Dynamics of spermiogenesis in Drosophila melanogaster. IV. Nuclear transformation. J Ultrastruct Res. 1974 Aug;48(2):284–303. doi: 10.1016/s0022-5320(74)80083-3. [DOI] [PubMed] [Google Scholar]