Mutation in a Structural Gene for a Beta-tubulin Specific to Testis in Drosophila Melanogaster

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1979 Aug 1

PMID 115008

Citations 53

Authors

K J Kemphues

R A Raff

T C Kaufman

E C Raff

Affiliations

Soon will be listed here.

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.

Citing Articles

The evolutionarily conserved PhLP3 is essential for sperm development in Drosophila melanogaster.

Petit C, Kojak E, Webster S, Marra M, Sweeney B, Chaikin C PLoS One. 2024; 19(10):e0306676.

PMID: 39480878 PMC: 11527243. DOI: 10.1371/journal.pone.0306676.

The tubulin database: Linking mutations, modifications, ligands and local interactions.

Abbaali I, Truong D, Day S, Mushayeed F, Ganesh B, Haro-Ramirez N PLoS One. 2023; 18(12):e0295279.

PMID: 38064432 PMC: 10707541. DOI: 10.1371/journal.pone.0295279.

The Tubulin Superfamily in Apicomplexan Parasites.

Morrissette N, Abbaali I, Ramakrishnan C, Hehl A Microorganisms. 2023; 11(3).

PMID: 36985278 PMC: 10056924. DOI: 10.3390/microorganisms11030706.

The Tubulin Code in Microtubule Dynamics and Information Encoding.

Roll-Mecak A Dev Cell. 2020; 54(1):7-20.

PMID: 32634400 PMC: 11042690. DOI: 10.1016/j.devcel.2020.06.008.

Identification of genes for engineering the male germline of Aedes aegypti and Ceratitis capitata.

Sutton E, Yu Y, Shimeld S, White-Cooper H, Alphey A BMC Genomics. 2016; 17(1):948.

PMID: 27871244 PMC: 5117610. DOI: 10.1186/s12864-016-3280-3.

References

Fulton C, Kowit J . Programmed synthesis of flagellar tubulin during cell differentiation in Naegleria. Ann N Y Acad Sci. 1975; 253:318-32. DOI: 10.1111/j.1749-6632.1975.tb19210.x. View

Waring G, Allis C, Mahowald A . Isolation of polar granules and the identification of polar granule-specific protein. Dev Biol. 1978; 66(1):197-206. DOI: 10.1016/0012-1606(78)90284-1. View

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; 69(2):301-12. PMC: 2109694. DOI: 10.1083/jcb.69.2.301. View

Stephens R . Differential protein synthesis and utilization during cilia formation in sea urchin embryos. Dev Biol. 1977; 61(2):311-29. DOI: 10.1016/0012-1606(77)90301-3. View

BEADLE G, EPHRUSSI B . The Differentiation of Eye Pigments in Drosophila as Studied by Transplantation. Genetics. 1936; 21(3):225-47. PMC: 1208671. DOI: 10.1093/genetics/21.3.225. View

OFarrell P, Goodman H, Ofarrell P . High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 1977; 12(4):1133-41. DOI: 10.1016/0092-8674(77)90176-3. View

Cleveland D, Fischer S, Kirschner M, Laemmli U . Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977; 252(3):1102-6. View

Lai M, Morris N . Identification of a gene for beta-tubulin in Aspergillus nidulans. Cell. 1978; 15(2):639-47. DOI: 10.1016/0092-8674(78)90032-6. View

Lifschytz E, Hareven D . Gene expression and the control of spermatid morphogenesis in Drosophila melanogaster. Dev Biol. 1977; 58(2):276-94. DOI: 10.1016/0012-1606(77)90092-6. View

10.

Lifschytz E, Meyer G . Characterisation of male meiotic-sterile mutations in drosophila melanogaster. The genetic control of meiotic divisions and gametogenesis. Chromosoma. 1977; 64(4):371-92. DOI: 10.1007/BF00294944. View

11.

Kowit J, Fulton C . Purification and properties of flagellar outer doublet tubulin from Naegleria gruberi and a radioimmune assay for tubulin. J Biol Chem. 1974; 249(11):3638-46. View

12.

Wilkinson R, Stanley H, BOWMAN J . 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; 48(2):242-58. DOI: 10.1016/s0022-5320(74)80080-8. View

13.

Kowit J, 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; 71(7):2877-81. PMC: 388575. DOI: 10.1073/pnas.71.7.2877. View

14.

Olmsted J, 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; 65(1):129-36. PMC: 286201. DOI: 10.1073/pnas.65.1.129. View

15.

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

16.

Kiefer B . Development, organization, and degeneration of the Drosophila sperm flagellum. J Cell Sci. 1970; 6(1):177-94. DOI: 10.1242/jcs.6.1.177. View

17.

Rungger-Brandle E . Morphogenetic deficiencies in transplanted gonadal anlagen of the mutant l(3)pl (lethal-polyploid) in Drosophila hydei. Exp Cell Res. 1977; 107(2):301-12. DOI: 10.1016/0014-4827(77)90353-6. View

18.

. Abnormal microtubules in testes of the mutant l(3)pl (lethal-polyploid) of Drosophila hydei, cultured in vivo. Exp Cell Res. 1977; 107(2):313-24. DOI: 10.1016/0014-4827(77)90354-8. View

19.

Stephens R . Primary structural differences among tubulin subunits from flagella, cilia, and the cytoplasm. Biochemistry. 1978; 17(14):2882-91. DOI: 10.1021/bi00607a029. View

20.

Bibring T, BAXANDALL J . Peptide analysis by isoelectric focusing in polyacrylamide gels. Anal Biochem. 1978; 85(1):1-14. DOI: 10.1016/0003-2697(78)90266-x. View