Abstract
Studies of the abnormal oocyte (abo) gene of Drosophila melanogaster have previously been limited to the analysis of a single mutant allele, abnormal oocyte(1) (abo(1)). The abo(1) mutation causes a maternal-effect lethality that can be partially rescued zygotically by the abo(+) allele and by increasing the dosage of specific regions of heterochromatin denoted ABO. This report describes the properties of abo(2), a new P-element-induced allele that allowed us to reexamine the nature of maternal-effect defect. Comparisons of the phenotype of progeny of abo(1)/abo(1) and abo(1)/abo(2) females show that the preblastoderm lethality previously described as a component of the abo mutant maternal effect results from a recessive fertilization defect associated with the abo(1) chromosome. We demonstrate here that the abo-induced maternal effect lethality occurs predominately late in embryogenesis after cuticle deposition but before hatching. The phenocritical period for zygotic rescue by heterochromatin coincides with this period of late embryogenesis. We have used the abo(2) mutation to map and molecularly clone the gene. We show that the abo gene is located in the 32C cytogenetic interval and identify the putative abo transcript from mRNA isolated from adult females. Using germline transformation, we show that a 9-kb genomic fragment to which the transcript maps, partially fulfills requirement for maternal and zygotic abo(+) function.
Full Text
The Full Text of this article is available as a PDF (3.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson K. V., Lengyel J. A. Rates of synthesis of major classes of RNA in Drosophila embryos. Dev Biol. 1979 May;70(1):217–231. doi: 10.1016/0012-1606(79)90018-6. [DOI] [PubMed] [Google Scholar]
- Bourouis M., Richards G. Remote regulatory sequences of the Drosophila glue gene sgs3 as revealed by P-element transformation. Cell. 1985 Feb;40(2):349–357. doi: 10.1016/0092-8674(85)90149-7. [DOI] [PubMed] [Google Scholar]
- Corces V. G., Geyer P. K. Interactions of retrotransposons with the host genome: the case of the gypsy element of Drosophila. Trends Genet. 1991 Mar;7(3):86–90. doi: 10.1016/0168-9525(91)90277-W. [DOI] [PubMed] [Google Scholar]
- Edgar B. A., Schubiger G. Parameters controlling transcriptional activation during early Drosophila development. Cell. 1986 Mar 28;44(6):871–877. doi: 10.1016/0092-8674(86)90009-7. [DOI] [PubMed] [Google Scholar]
- Gatti M., Pimpinelli S. Functional elements in Drosophila melanogaster heterochromatin. Annu Rev Genet. 1992;26:239–275. doi: 10.1146/annurev.ge.26.120192.001323. [DOI] [PubMed] [Google Scholar]
- Graziani F., Vicari L., Boncinelli E., Malva C., Manzi A., Mariani C. Selective replication of ribosomal DNA repeats after loss of the abnormal oocyte phenotype in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7662–7664. doi: 10.1073/pnas.78.12.7662. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karr T. L. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech Dev. 1991 Jun;34(2-3):101–111. doi: 10.1016/0925-4773(91)90047-a. [DOI] [PubMed] [Google Scholar]
- Krider H. M., Levine B. I. Studies on the mutation abnormal oocyte and its interaction with the ribosomal DNA of Drosophila melanogaster. Genetics. 1975 Nov;81(3):501–513. doi: 10.1093/genetics/81.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krider H. M., Yedvobnick B., Levine B. I. The effect of abo phenotypic expression on ribosomal DNA instabilities in Drosophila melanogaster. Genetics. 1979 Jul;92(3):879–889. doi: 10.1093/genetics/92.3.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lamb M. M., Laird C. D. Increase in nuclear poly(A)-containing RNA at syncytial blastoderm in Drosophila melanogaster embryos. Dev Biol. 1976 Aug;52(1):31–42. doi: 10.1016/0012-1606(76)90004-x. [DOI] [PubMed] [Google Scholar]
- Laski F. A., Rio D. C., Rubin G. M. Tissue specificity of Drosophila P element transposition is regulated at the level of mRNA splicing. Cell. 1986 Jan 17;44(1):7–19. doi: 10.1016/0092-8674(86)90480-0. [DOI] [PubMed] [Google Scholar]
- Laughon A., Boulet A. M., Bermingham J. R., Jr, Laymon R. A., Scott M. P. Structure of transcripts from the homeotic Antennapedia gene of Drosophila melanogaster: two promoters control the major protein-coding region. Mol Cell Biol. 1986 Dec;6(12):4676–4689. doi: 10.1128/mcb.6.12.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lavorgna G., Malva C., Manzi A., Gigliotti S., Graziani F. The abnormal oocyte phenotype is correlated with the presence of blood transposon in Drosophila melanogaster. Genetics. 1989 Nov;123(3):485–494. doi: 10.1093/genetics/123.3.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee C. S., Curtis D., McCarron M., Love C., Gray M., Bender W., Chovnick A. Mutations affecting expression of the rosy locus in Drosophila melanogaster. Genetics. 1987 May;116(1):55–66. doi: 10.1093/genetics/116.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
- McKnight S. L., Miller O. L., Jr Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell. 1976 Jun;8(2):305–319. doi: 10.1016/0092-8674(76)90014-3. [DOI] [PubMed] [Google Scholar]
- Mitchison T. J., Sedat J. Localization of antigenic determinants in whole Drosophila embryos. Dev Biol. 1983 Sep;99(1):261–264. doi: 10.1016/0012-1606(83)90275-0. [DOI] [PubMed] [Google Scholar]
- O'Hare K., Rubin G. M. Structures of P transposable elements and their sites of insertion and excision in the Drosophila melanogaster genome. Cell. 1983 Aug;34(1):25–35. doi: 10.1016/0092-8674(83)90133-2. [DOI] [PubMed] [Google Scholar]
- Parry D. M., Sandler L. The genetic identification of a heterochromatic segment on the X chromosome of Drosophila melanogaster. Genetics. 1974 Jul;77(3):535–539. doi: 10.1093/genetics/77.3.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pimpinelli S., Sullivan W., Prout M., Sandler L. On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics. 1985 Apr;109(4):701–724. doi: 10.1093/genetics/109.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. doi: 10.1016/b978-0-409-90042-2.50028-3. [DOI] [PubMed] [Google Scholar]
- 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]
- Sandler L. Evidence for a set of closely linked autosomal genes that interact with sex-chromosome heterochromatin in Drosophila melanogaster. Genetics. 1977 Jul;86(3):567–582. doi: 10.1093/genetics/86.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sandler L. The Regulation of Sex Chromosome Heterochromatic Activity by an Autosomal Gene in DROSOPHILA MELANOGASTER. Genetics. 1970 Mar;64(3-4):481–493. doi: 10.1093/genetics/64.3-4.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schultz J. Variegation in Drosophila and the Inert Chromosome Regions. Proc Natl Acad Sci U S A. 1936 Jan;22(1):27–33. doi: 10.1073/pnas.22.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simon J. A., Sutton C. A., Lobell R. B., Glaser R. L., Lis J. T. Determinants of heat shock-induced chromosome puffing. Cell. 1985 Apr;40(4):805–817. doi: 10.1016/0092-8674(85)90340-x. [DOI] [PubMed] [Google Scholar]
- Sullivan W., Pimpinelli S. The genetic factors altered in homozygous abo stocks of Drosophila melanogaster. Genetics. 1986 Nov;114(3):885–895. doi: 10.1093/genetics/114.3.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tomkiel J., Pimpinelli S., Sandler L. Rescue from the abnormal oocyte maternal-effect lethality by ABO heterochromatin in Drosophila melanogaster. Genetics. 1991 Jul;128(3):583–594. doi: 10.1093/genetics/128.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yedvobnick B., Krider H. M., Levine B. I. Analysis of the autosomal mutation abo and its interaction with the ribosomal DNA or Drosophila melanogaster: the role of X-chromosome heterochromatin. Genetics. 1980 Jul;95(3):661–672. doi: 10.1093/genetics/95.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zalokar M. Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol. 1976 Apr;49(2):425–437. doi: 10.1016/0012-1606(76)90185-8. [DOI] [PubMed] [Google Scholar]