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. 1990 May;125(1):77–90. doi: 10.1093/genetics/125.1.77

Interacting Genes That Affect Microtubule Function in Drosophila Melanogaster: Two Classes of Mutation Revert the Failure to Complement between Hay(nc2) and Mutations in Tubulin Genes

C L Regan 1, M T Fuller 1
PMCID: PMC1204010  PMID: 2111265

Abstract

The recessive male sterile mutation hay(nc2) of Drosophila melanogaster fails to complement certain β(2)-tubulin and α-tubulin mutations, suggesting that the haywire product plays a role in microtubule function, perhaps as a structural component of microtubules. The genetic interaction appears to require the presence of the aberrant product encoded by hay(nc2), which may act as a structural poison. Based on this observation, we have isolated ten new mutations that revert the failure to complement between hay(nc2) and B2t(n). The revertants tested behaved as intragenic mutations of hay in recombination tests, and fell into two phenotypic classes, suggesting two functional domains of the hay gene product. Some revertants were hemizygous viable and less severe than hay(nc2) in their recessive phenotype. These mutations might revert the poison by restoring the aberrant product encoded by the hay(nc2) allele to more wild-type function. Most of the revertants were recessive lethal mutations, indicating that the hay gene product is essential for viability. These more extreme mutations could revert the poison by destroying the ability of the aberrant haywire(nc2) product to interact structurally with microtubules. Flies heterozygous for the original hay(nc2) allele and an extreme revertant show defects in both the structure and the function of the male meiotic spindle.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aizawa H., Murofushi H., Kotani S., Hisanaga S., Hirokawa N., Sakai H. Limited chymotryptic digestion of bovine adrenal 190,000-Mr microtubule-associated protein and preparation of a 27,000-Mr fragment which stimulates microtubule assembly. J Biol Chem. 1987 Mar 15;262(8):3782–3787. [PubMed] [Google Scholar]
  2. Brenner S. L., Liaw L. H., Berns M. W. Laser microirradiation of kinetochores in mitotic PtK2 cells: chromatid separation and micronucleus formation. Cell Biophys. 1980 Jun;2(2):139–152. doi: 10.1007/BF02795840. [DOI] [PubMed] [Google Scholar]
  3. González C., Casal J., Ripoll P. Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. Genet Res. 1989 Dec;54(3):205–212. doi: 10.1017/s0016672300028664. [DOI] [PubMed] [Google Scholar]
  4. Hays T. S., Deuring R., Robertson B., Prout M., Fuller M. T. Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene of Drosophila melanogaster. Mol Cell Biol. 1989 Mar;9(3):875–884. doi: 10.1128/mcb.9.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hirokawa N., Shiomura Y., Okabe S. Tau proteins: the molecular structure and mode of binding on microtubules. J Cell Biol. 1988 Oct;107(4):1449–1459. doi: 10.1083/jcb.107.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Kalfayan L., Wensink P. C. Developmental regulation of Drosophila alpha-tubulin genes. Cell. 1982 May;29(1):91–98. doi: 10.1016/0092-8674(82)90093-9. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Lohka M. J., Masui Y. Roles of cytosol and cytoplasmic particles in nuclear envelope assembly and sperm pronuclear formation in cell-free preparations from amphibian eggs. J Cell Biol. 1984 Apr;98(4):1222–1230. doi: 10.1083/jcb.98.4.1222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ludueńa R. F., Shooter E. M., Wilson L. Structure of the tubulin dimer. J Biol Chem. 1977 Oct 25;252(20):7006–7014. [PubMed] [Google Scholar]
  11. Matthews K. A., Kaufman T. C. Developmental consequences of mutations in the 84B alpha-tubulin gene of Drosophila melanogaster. Dev Biol. 1987 Jan;119(1):100–114. doi: 10.1016/0012-1606(87)90211-9. [DOI] [PubMed] [Google Scholar]
  12. Matthews K. A., Miller D. F., Kaufman T. C. Developmental distribution of RNA and protein products of the Drosophila alpha-tubulin gene family. Dev Biol. 1989 Mar;132(1):45–61. doi: 10.1016/0012-1606(89)90203-0. [DOI] [PubMed] [Google Scholar]
  13. Murofushi H., Kotani S., Aizawa H., Hisanaga S., Hirokawa N., Sakai H. Purification and characterization of a 190-kD microtubule-associated protein from bovine adrenal cortex. J Cell Biol. 1986 Nov;103(5):1911–1919. doi: 10.1083/jcb.103.5.1911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell. 1987 Jan 30;48(2):205–217. doi: 10.1016/0092-8674(87)90424-7. [DOI] [PubMed] [Google Scholar]
  15. Olmsted J. B. Microtubule-associated proteins. Annu Rev Cell Biol. 1986;2:421–457. doi: 10.1146/annurev.cb.02.110186.002225. [DOI] [PubMed] [Google Scholar]
  16. Piperno G., Fuller M. T. Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J Cell Biol. 1985 Dec;101(6):2085–2094. doi: 10.1083/jcb.101.6.2085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Regan C. L., Fuller M. T. Interacting genes that affect microtubule function: the nc2 allele of the haywire locus fails to complement mutations in the testis-specific beta-tubulin gene of Drosophila. Genes Dev. 1988 Jan;2(1):82–92. doi: 10.1101/gad.2.1.82. [DOI] [PubMed] [Google Scholar]
  18. Stearns T., Botstein D. Unlinked noncomplementation: isolation of new conditional-lethal mutations in each of the tubulin genes of Saccharomyces cerevisiae. Genetics. 1988 Jun;119(2):249–260. doi: 10.1093/genetics/119.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vallee R. Structure and phosphorylation of microtubule-associated protein 2 (MAP 2). Proc Natl Acad Sci U S A. 1980 Jun;77(6):3206–3210. doi: 10.1073/pnas.77.6.3206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Voter W. A., Erickson H. P. Electron microscopy of MAP 2 (microtubule-associated protein 2). J Ultrastruct Res. 1982 Sep;80(3):374–382. doi: 10.1016/s0022-5320(82)80051-8. [DOI] [PubMed] [Google Scholar]
  21. Yang J. T., Laymon R. A., Goldstein L. S. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses. Cell. 1989 Mar 10;56(5):879–889. doi: 10.1016/0092-8674(89)90692-2. [DOI] [PubMed] [Google Scholar]

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