Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1995 May;140(1):219–229. doi: 10.1093/genetics/140.1.219

Genetic Characterization of Ms(3)k81, a Paternal Effect Gene of Drosophila Melanogaster

G K Yasuda 1, G Schubiger 1, B T Wakimoto 1
PMCID: PMC1206549  PMID: 7635287

Abstract

The vast majority of known male sterile mutants of Drosophila melanogaster fail to produce mature sperm or mate properly. The ms(3)K81(1) mutation is one of a rare class of male sterile mutations in which sterility is caused by developmental arrest after sperm entry into the egg. Previous studies showed that males homozygous for the K81(1) mutation produce progeny that arrest at either of two developmental stages. Most embryos arrest during early nuclear cycles, whereas the remainder are haploid embryos that arrest at a later stage. This description of the mutant phenotype was based on the analysis of a single allele isolated from a natural population. It was therefore unclear whether this unique paternal effect phenotype reflected the normal function of the gene. The genetic analysis and initial molecular characterization of five new K81 mutations are described here. Hemizygous conditions and heteroallelic combinations of the alleles were associated with male sterility caused by defects in embryogenesis. No other mutant phenotypes were observed. Thus, the K81 gene acted as a strict paternal effect gene. Moreover, the biphasic pattern of developmental arrest was common to all the alleles. These findings strongly suggested that the unusual embryonic phenotype caused by all five new alleles was due to loss of function of the K81(+) gene. The K81 gene is therefore the first clear example of a strict paternal effect gene in Drosophila. Based on the embryonic lethal phenotypes, we suggest that the K81(+) gene encodes a sperm-specific product that is essential for the male pronucleus to participate in the first few embryonic nuclear divisions.

Full Text

The Full Text of this article is available as a PDF (5.4 MB).

Selected References

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

  1. Baker J., Theurkauf W. E., Schubiger G. Dynamic changes in microtubule configuration correlate with nuclear migration in the preblastoderm Drosophila embryo. J Cell Biol. 1993 Jul;122(1):113–121. doi: 10.1083/jcb.122.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bakken A. H. A cytological and genetic study of oogenesis in Drosophila melanogaster. Dev Biol. 1973 Jul;33(1):100–122. doi: 10.1016/0012-1606(73)90167-x. [DOI] [PubMed] [Google Scholar]
  3. Bender W., Spierer P., Hogness D. S. Chromosomal walking and jumping to isolate DNA from the Ace and rosy loci and the bithorax complex in Drosophila melanogaster. J Mol Biol. 1983 Jul 25;168(1):17–33. doi: 10.1016/s0022-2836(83)80320-9. [DOI] [PubMed] [Google Scholar]
  4. CRAWLEY J. C. CYTOPLASMIC FINE STRUCTURE IN ACETABULARIA. Exp Cell Res. 1964 Sep;35:507–514. doi: 10.1016/0014-4827(64)90138-7. [DOI] [PubMed] [Google Scholar]
  5. Castrillon D. H., Gönczy P., Alexander S., Rawson R., Eberhart C. G., Viswanathan S., DiNardo S., Wasserman S. A. Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics. 1993 Oct;135(2):489–505. doi: 10.1093/genetics/135.2.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Edgar B. A., Kiehle C. P., Schubiger G. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell. 1986 Jan 31;44(2):365–372. doi: 10.1016/0092-8674(86)90771-3. [DOI] [PubMed] [Google Scholar]
  7. Erdélyi M., Szabad J. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. I. Mutations on the third chromosome. Genetics. 1989 May;122(1):111–127. doi: 10.1093/genetics/122.1.111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Freeman M., Glover D. M. The gnu mutation of Drosophila causes inappropriate DNA synthesis in unfertilized and fertilized eggs. Genes Dev. 1987 Nov;1(9):924–930. doi: 10.1101/gad.1.9.924. [DOI] [PubMed] [Google Scholar]
  9. Gönczy P., Viswanathan S., DiNardo S. Probing spermatogenesis in Drosophila with P-element enhancer detectors. Development. 1992 Jan;114(1):89–98. doi: 10.1242/dev.114.1.89. [DOI] [PubMed] [Google Scholar]
  10. Hackstein J. H. Spermatogenesis in Drosophila. A genetic approach to cellular and subcellular differentiation. Eur J Cell Biol. 1991 Dec;56(2):151–169. [PubMed] [Google Scholar]
  11. Hill D. P., Shakes D. C., Ward S., Strome S. A sperm-supplied product essential for initiation of normal embryogenesis in Caenorhabditis elegans is encoded by the paternal-effect embryonic-lethal gene, spe-11. Dev Biol. 1989 Nov;136(1):154–166. doi: 10.1016/0012-1606(89)90138-3. [DOI] [PubMed] [Google Scholar]
  12. Karsch-Mizrachi I., Haynes S. R. The Rb97D gene encodes a potential RNA-binding protein required for spermatogenesis in Drosophila. Nucleic Acids Res. 1993 May 11;21(9):2229–2235. doi: 10.1093/nar/21.9.2229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Knibb W. R., Tearle R. G., Elizur A., Saint R. Genetic analysis of chromosomal region 97D2-9 of Drosophila melanogaster. Mol Gen Genet. 1993 May;239(1-2):109–114. doi: 10.1007/BF00281608. [DOI] [PubMed] [Google Scholar]
  14. Lin H. F., Wolfner M. F. The Drosophila maternal-effect gene fs(1)Ya encodes a cell cycle-dependent nuclear envelope component required for embryonic mitosis. Cell. 1991 Jan 11;64(1):49–62. doi: 10.1016/0092-8674(91)90208-g. [DOI] [PubMed] [Google Scholar]
  15. Longo F. J. Fertilization: a comparative ultrastructural review. Biol Reprod. 1973 Sep;9(2):149–215. doi: 10.1093/biolreprod/9.2.149. [DOI] [PubMed] [Google Scholar]
  16. Mains P. E., Kemphues K. J., Sprunger S. A., Sulston I. A., Wood W. B. Mutations affecting the meiotic and mitotic divisions of the early Caenorhabditis elegans embryo. Genetics. 1990 Nov;126(3):593–605. doi: 10.1093/genetics/126.3.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Poccia D. L., Green G. R. Packaging and unpackaging the sea urchin sperm genome. Trends Biochem Sci. 1992 Jun;17(6):223–227. doi: 10.1016/0968-0004(92)90382-J. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Poccia D. Remodeling of nucleoproteins during gametogenesis, fertilization, and early development. Int Rev Cytol. 1986;105:1–65. doi: 10.1016/s0074-7696(08)61061-x. [DOI] [PubMed] [Google Scholar]
  19. Robbins L. G., Pimpinelli S. Chromosome damage and early developmental arrest caused by the Rex element of Drosophila melanogaster. Genetics. 1994 Oct;138(2):401–411. doi: 10.1093/genetics/138.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Robertson H. M., Preston C. R., Phillis R. W., Johnson-Schlitz D. M., Benz W. K., Engels W. R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics. 1988 Mar;118(3):461–470. doi: 10.1093/genetics/118.3.461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Russell S. R., Kaiser K. Drosophila melanogaster male germ line-specific transcripts with autosomal and Y-linked genes. Genetics. 1993 May;134(1):293–308. doi: 10.1093/genetics/134.1.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Santamaria P. Analysis of haploid mosaics in Drosophila. Dev Biol. 1983 Apr;96(2):285–295. doi: 10.1016/0012-1606(83)90165-3. [DOI] [PubMed] [Google Scholar]
  23. Schatten G., Schatten H. Fertilization: motility, the cytoskeleton and the nuclear architecture. Oxf Rev Reprod Biol. 1987;9:322–378. [PubMed] [Google Scholar]
  24. Schüpbach T., Wieschaus E. Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics. 1989 Jan;121(1):101–117. doi: 10.1093/genetics/121.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shamanski F. L., Orr-Weaver T. L. The Drosophila plutonium and pan gu genes regulate entry into S phase at fertilization. Cell. 1991 Sep 20;66(6):1289–1300. doi: 10.1016/0092-8674(91)90050-9. [DOI] [PubMed] [Google Scholar]
  26. Sullivan W., Fogarty P., Theurkauf W. Mutations affecting the cytoskeletal organization of syncytial Drosophila embryos. Development. 1993 Aug;118(4):1245–1254. doi: 10.1242/dev.118.4.1245. [DOI] [PubMed] [Google Scholar]
  27. Szabad J., Erdélyi M., Hoffmann G., Szidonya J., Wright T. R. Isolation and characterization of dominant female sterile mutations of Drosophila melanogaster. II. Mutations on the second chromosome. Genetics. 1989 Aug;122(4):823–835. doi: 10.1093/genetics/122.4.823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  29. Tomlinson A., Kimmel B. E., Rubin G. M. rough, a Drosophila homeobox gene required in photoreceptors R2 and R5 for inductive interactions in the developing eye. Cell. 1988 Dec 2;55(5):771–784. doi: 10.1016/0092-8674(88)90133-x. [DOI] [PubMed] [Google Scholar]
  30. Tower J., Karpen G. H., Craig N., Spradling A. C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 1993 Feb;133(2):347–359. doi: 10.1093/genetics/133.2.347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Underwood E. M., Briot A. S., Doll K. Z., Ludwiczak R. L., Otteson D. C., Tower J., Vessey K. B., Yu K. Genetics of 51D-52A, a region containing several maternal-effect genes and two maternal-specific transcripts in Drosophila. Genetics. 1990 Nov;126(3):639–650. doi: 10.1093/genetics/126.3.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Yasuda G. K., Baker J., Schubiger G. Independent roles of centrosomes and DNA in organizing the Drosophila cytoskeleton. Development. 1991 Feb;111(2):379–391. doi: 10.1242/dev.111.2.379. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES