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. 1979 Aug;76(8):3991–3995. doi: 10.1073/pnas.76.8.3991

Mutation in a structural gene for a beta-tubulin specific to testis in Drosophila melanogaster.

K J Kemphues, R A Raff, T C Kaufman, E C Raff
PMCID: PMC383962  PMID: 115008

Abstract

By two-dimensional gel electrophoresis of tubulins prepared from tissues of Drosophila melanogaster we have identified a beta-tubulin subunit that is present only in the testis. Furthermore, we have isolated, as a male sterile, a third chromosome dominant mutation [ms(3)KKD] in the structural gene for this beta-tubulin. Males heterozygous for this mutation produce no motile spermatozoa. Beginning with meiosis, all processes in spermatogenesis are abnormal to some extent. Many microtubules (including both cytoplasmic microtubules and doublet tubules of the axoneme) show aberrant structure in cross section, and the overall morphology of the developing spermatids is disorganized. Testes from these males were shown, by two-dimensional gel electrophoresis, to contain both the normal testis-specific beta-tubulin and an electrophoretic variant of this tubulin in equal amounts. Both wild-type and mutant testis-specific beta-tubulins were characterized by vinblastine sulfate precipitation, coassembly with purified Drosophila embryo tubulin, and peptide mapping.

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Selected References

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  1. Beadle G. W., Ephrussi B. The Differentiation of Eye Pigments in Drosophila as Studied by Transplantation. Genetics. 1936 May;21(3):225–247. doi: 10.1093/genetics/21.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bibring T., Baxandall J., Denslow S., Walker B. Heterogeneity of the alpha subunit of tubulin and the variability of tubulin within a single organism. J Cell Biol. 1976 May;69(2):301–312. doi: 10.1083/jcb.69.2.301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bibring T., Baxandall J. Peptide analysis by isoelectric focusing in polyacrylamide gels. Anal Biochem. 1978 Mar;85(1):1–14. doi: 10.1016/0003-2697(78)90266-x. [DOI] [PubMed] [Google Scholar]
  4. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  5. Duncan I. W., Kaufman T. C. Cytogenic analysis of chromosome 3 in Drosophila melanogaster: mapping of the proximal portion of the right arm. Genetics. 1975 Aug;80(4):733–752. doi: 10.1093/genetics/80.4.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fulton C., Kowit J. D. Programmed synthesis of flagellar tubulin during cell differentiation in Naegleria. Ann N Y Acad Sci. 1975 Jun 30;253:318–332. doi: 10.1111/j.1749-6632.1975.tb19210.x. [DOI] [PubMed] [Google Scholar]
  7. Green L. H., Brandis J. W., Turner F. R., Raff R. A. Cytoplasmic microtubule proteins of the embryo of Drosophila melanogaster. Biochemistry. 1975 Oct 7;14(20):4487–4491. doi: 10.1021/bi00691a023. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Kowit J. D., Fulton C. Programmed synthesis of tubulin for the flagella that develop during cell differentiation in Naegleria gruberi. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2877–2881. doi: 10.1073/pnas.71.7.2877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kowit J. D., Fulton C. Purification and properties of flagellar outer doublet tubulin from Naegleria gruberi and a radioimmune assay for tubulin. J Biol Chem. 1974 Jun 10;249(11):3638–3646. [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. Lifschytz E., Hareven D. Gene expression and the control of spermatid morphogenesis in Drosophila melanogaster. Dev Biol. 1977 Jul 15;58(2):276–294. doi: 10.1016/0012-1606(77)90092-6. [DOI] [PubMed] [Google Scholar]
  13. Lifschytz E., Meyer G. F. Characterisation of male meiotic-sterile mutations in drosophila melanogaster. The genetic control of meiotic divisions and gametogenesis. Chromosoma. 1977 Dec 6;64(4):371–392. doi: 10.1007/BF00294944. [DOI] [PubMed] [Google Scholar]
  14. O'Farrell P. Z., Goodman H. M., O'Farrell P. H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 1977 Dec;12(4):1133–1141. doi: 10.1016/0092-8674(77)90176-3. [DOI] [PubMed] [Google Scholar]
  15. Olmsted J. B., Carlson K., Klebe R., Ruddle F., Rosenbaum J. Isolation of microtubule protein from cultured mouse neuroblastoma cells. Proc Natl Acad Sci U S A. 1970 Jan;65(1):129–136. doi: 10.1073/pnas.65.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rungger-Brändle E. Morphogenetic deficiencies in transplanted gonadal anlagen of the mutant l(3)pl (lethal-polyploid) in Drosophila hydei. Exp Cell Res. 1977 Jul;107(2):301–312. doi: 10.1016/0014-4827(77)90353-6. [DOI] [PubMed] [Google Scholar]
  17. Rungger-Brändle V. E. Abnormal microtubules in testes of the mutant l(3)pl (lethal-polyploid) of Drosophila hydei, cultured in vivo. Exp Cell Res. 1977 Jul;107(2):313–324. doi: 10.1016/0014-4827(77)90354-8. [DOI] [PubMed] [Google Scholar]
  18. Sheir-Neiss G., Lai M. H., Morris N. R. Identification of a gene for beta-tubulin in Aspergillus nidulans. Cell. 1978 Oct;15(2):639–647. doi: 10.1016/0092-8674(78)90032-6. [DOI] [PubMed] [Google Scholar]
  19. Stephens R. E. Differential protein synthesis and utilization during cilia formation in sea urchin embryos. Dev Biol. 1977 Dec;61(2):311–329. doi: 10.1016/0012-1606(77)90301-3. [DOI] [PubMed] [Google Scholar]
  20. Stephens R. E. Primary structural differences among tubulin subunits from flagella, cilia, and the cytoplasm. Biochemistry. 1978 Jul 11;17(14):2882–2891. doi: 10.1021/bi00607a029. [DOI] [PubMed] [Google Scholar]
  21. Waring G. L., Allis C. D., Mahowald A. P. Isolation of polar granules and the identification of polar granule-specific protein. Dev Biol. 1978 Sep;66(1):197–206. doi: 10.1016/0012-1606(78)90284-1. [DOI] [PubMed] [Google Scholar]
  22. Wilkinson R. F., Stanley H. P., Bowman J. T. Genetic control of spermiogenesis in Drosophila melanogaster: the effects of abnormal cytoplasmic microtubule populations in mutant ms(3)10R and its colcemid-induced phenocopy. J Ultrastruct Res. 1974 Aug;48(2):242–258. doi: 10.1016/s0022-5320(74)80080-8. [DOI] [PubMed] [Google Scholar]

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