Skip to main content
SpringerLink
Log in

Cloning and analysis of fs(1) Ya, a maternal effect gene required for the initiation of Drosophila embryogenesis

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

The maternal effect locus fs(1) Ya is required for the fusion of the apposed sperm and egg pronuclei (syngamy) following fertilization in Drosophila. It is tightly linked to another complementation group, fs(1) Yb, needed for both oogenesis and embryogenesis. We have isolated a set of overlapping cloned sequences in the 3B4-6 region of the X chromosome encompassing the fs(1) Ya-fs(1) Yb region. A single 2.4 kb maternal transcript is encoded with-in this region, and an 8.5 kb DNA fragment that contains this transcript complements both fs(1) Ya and fs(1) Yb mutations. Northern and in situ hybridization analyses show that the maternal transcript is only present in nurse cells and oocytes beginning in previtellogenic stages, and is evenly distributed in the cytoplasm of 0–2 h syncytial embryos. The transcript is not detected in later stages of embryonic development. This expression pattern correlates closely with the genetic and developmental characteristics expected of the fs(1) Ya gene product.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ambrosio L, Schedl P (1984) Gene expression during Drosophila melanogaster oogenesis: Analysis by in situ hybridization to tissue sections. Dev Biol 105:80–92

    Google Scholar 

  • Anderson KV, Lengyel JA (1981) Changing rates of DNA and RNA synthesis in Drosophila embryos. Dev Biol 82:127–138

    Google Scholar 

  • Anderson KV, Lengyel JA (1984) Histone gene expression in Drosophila development: Multiple levels of gene regulation. In: Stein G, Stein J, Marzluff W (eds) Histone genes: Structure, organization, and regulation. John Wiley and Sons, New York, pp 135–161

    Google Scholar 

  • Anderson KV, Nüsslein-Volhard C (1984a) Genetic analysis of dorsal ventral embryonic pattern in Drosophila. In: Malacinski GM, Bryant S (eds) Pattern formation. Macmillan Publishing Co, New York, pp 269–289

    Google Scholar 

  • Anderson KV, Nüsslein-Volhard C (1984b) Information for the dorsal-ventral pattern of the Drosophila embryo is stored as mRNA. Nature 311:223–227

    Google Scholar 

  • Baker BS (1973) The maternal and zygotic control of development by cinnamon, a new mutant in Drosophila melanogaster. Dev Biol 33:429–440

    Google Scholar 

  • Belote JM, Handler AM, Wolfner MF, Livak KL, Baker BS (1985) Sex-specific regulation of yolk protein gene expression in Drosophila. Cell 40:339–348

    Google Scholar 

  • Bialojan S, Falkenberg D, Renkawitz-Pohl R (1984) Characterization and developmental expression of β-tubulin genes in Drosophila melanogaster. EMBO J 3:2543–2548

    Google Scholar 

  • Bond BJ, Davidson N (1986) The Drosophila melanogaster actin 5C gene uses two transcriptional initiation sites and three polyadenylation sites to express multiple mRNA species. Mol Cell Biol 6:2080–2088

    Google Scholar 

  • Boswell RE, Mahowald AP (1985) tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43:97–104

    Google Scholar 

  • Byers B, Goetsch L (1973) Duplication of spindle plaques and integration of the yeast cell cycle. Cold Spring Harbor Symp Quant Biol 38:123–131

    Google Scholar 

  • Byers B, Goetsch L (1975) Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol 124:511–523

    Google Scholar 

  • Cox KH, DeLeon DV, Angerer LM, Angerer RL (1984) Detection of mRNAs in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol 101:485–502

    Google Scholar 

  • Delgado MA, Conde J (1984) Benomyl prevents nuclear fusion in Saccharomyces cerevisiae. Mol Gen Genet 193:188–189

    Google Scholar 

  • DiBenedetto AJ, Lakich DM, Kruger WD, Belote JM, Baker BS, Wolfner MF (1987) Sequences expressed sex-specifically in Drosophila melanogaster adults. Dev Biol 119:242–251

    Google Scholar 

  • Edgar BA, Schubiger G (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44:871–877

    Google Scholar 

  • Favaloro J, Treisman R, Kamen R (1980) Transcriptional maps of Polyoma Virus-specific RNA: Analysis by two-dimensional nuclease S1 gel mapping. Methods Enzymol 65:718–749

    Google Scholar 

  • Feinberg AP, Vogelstein B (1984) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137:266–267

    Google Scholar 

  • Freeman M, Glover DM (1987) The gnu mutation of Drosophila causes inappropriate DNA synthesis in unfertilized and fertilized eggs. Genes Develop 1:924–930

    Google Scholar 

  • Freeman M, Nüsslein-Volhard C, Glover DM (1986) The dissociation of nuclear and centrosomal division in gnu, a mutation causing giant nuclei in Drosophila. Cell 46:457–468

    Google Scholar 

  • Gans M, Audit C, Masson M (1975) Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaser Genetics 81:683–704

    Google Scholar 

  • Gunaratne PH, Mansukhani A, Lipari SE, Liou H-C, Martindale DW, Goldberg ML (1986) Molecular cloning, germline transformation and transcriptional analysis of the zeste locus of Drosophila melanogaster. Proc Natl Acad Sci USA 83:701–705

    Google Scholar 

  • Hafen E, Levine M (1986) The localization of RNAs in Drosophila tissue sections by in situ hybridization. In: Roberts DB (ed) Drosophila: a practical approach. IRL Press, Oxford, pp 139–158

    Google Scholar 

  • Hu S-Y, Zhu C (1979) The fusion of male and female nuclei in fertilization of higher plants. Acta Bot Sinica 21:1–10

    Google Scholar 

  • Judd BH (1976) Genetic units of Drosophila — complex loci. In: Ashburner M, Novitski E (eds) The genetics and biology of Drosophila, vol 1 b. Academic Press, New York, pp 767–799

    Google Scholar 

  • Judd BH, Young MW (1973) An examination of the one cistron: one chromomere concept. Cold Spring Harbor Symp Quant Biol 38:573–579

    Google Scholar 

  • Klemenz R, Weber U, Gehring WJ (1987) The white gene as a marker in a new P-element vector for gene transfer in Drosophila. Nucleic Acids Res 15:3947–3959

    Google Scholar 

  • Komitopoulou KM, Gans M, Margaritis LH, Kafatos FC, Masson M (1983) Isolation and characterization of sex-linked female sterile mutants in Drosophila melanogaster with special attention to eggshell mutants. Genetics 105:897–920

    Google Scholar 

  • Lindsley D, Zimm G (1985) The genome of Drosophila melanogaster. Part 1: genes A-K Drosophila Inform Serv 62:133–137

    Google Scholar 

  • Lis JT, Simon JA, Sutton cA (1983) New heat shock puffs and β-galactosidase activity resulting from the transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell 35:403–410

    Google Scholar 

  • McKnight SL, Miller Jr OL (1976) Ultrstructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8:305–319

    Google Scholar 

  • Mahowald AP, Kambysellis MP (1980) Oogenesis. In: Ashburner M, Wright TRF (eds) The genetics and biology of Drosophila, vol 2d. Academic Press, New York, pp 141–224

    Google Scholar 

  • Maniatis T, Hardison RC, Lacy E, Lauer J, O'Connell C, Quon D, Sim GK, Efstradiatis A (1978) The isolation of structural genes from libraries of eukaryotic DNA. Cell 15:687–701

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Melton D, Krieg PA, Rebagliati MR, Maniatis T, Zinn K, green MR (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res 12:7035–7056

    Google Scholar 

  • Mlodzik M, Fjose A, Gehring WJ (1985) Isolation of caudal, a Drosophila melanogaster gene with maternal expression, whose transcripts form a concentration gradient at the pre-blastoderm stage. EMBO J 4:2961–2969

    Google Scholar 

  • Mohler D (1977) Developmental genetics of the Drosophila egg. I. Identification of 50 sex-linked cistrons with maternal effects on embryonic development. Genetics 85:259–272

    Google Scholar 

  • Mohler D, Carroll A (1984) Sex-linked female sterile mutations. Drosophila Inform Serv 60:236–272

    Google Scholar 

  • Mohler J, Wieschaus E (1985) Bicaudal mutations of Drosophila melanogaster: Alteration of blastoderm cell fate. Cold Spring Harbor Symp Quant Biol 50:105–111

    Google Scholar 

  • Mohler J, Wieschaus E (1986) Dominant maternal effect mutations of Drosophila melanogaster causing the production of doubleabdomen embryos. Genetics 112:803–822

    Google Scholar 

  • Nüsslein-Volhard C (1979) Maternal effect mutations that alter the spatial coordinates of the embryos of Drosophila melanogaster. In: Subtelny S, Koenigsberg IR (eds) Determinants of Spatial Organization. Academic Press, New York, pp 185–211

    Google Scholar 

  • Perrimon N, Mohler D, Engstrom L, Mahowald AP (1986) X-linked female-sterile loci in Drosophila melanogaster. Genetics 113:695–712

    Google Scholar 

  • Pirrotta V, Hadfield C, Pretorius GHJ (1983) Microdissection and cloning of the white locus and the 3B1-3C2 region of the Drosophila X chromosome. EMBO J 2:927–934

    Google Scholar 

  • Reddy P, Zehring WA, Wheeler DA, Pirrotta V, Hadfield C, Hall JC, Rosbash M (1984) Molecular analysis of the period locus in Drosophila melanogaster and identification of a transcript involved in biological rhythms. Cell 38:701–710

    Google Scholar 

  • Rubin GM, Spradling A (1983) Vectors for P element-mediated gene transfer in Drosophila. Nucleic Acids Res 11:6341–6351

    Google Scholar 

  • Russel M, Kidd S, Kelley MR (1986) An improved filamentous helper phage for generating single-stranded plasmid DNA. Gene 45:333–338

    Google Scholar 

  • Santamaría P (1984) Analysis of haploid mosaics in Drosophila. Dev Biol 96:285–295

    Google Scholar 

  • Santamaría P, Gans M (1980) Chimaeras of Drosophila melanogaster obtained by injection of haploid nuclei. Nature 287:143–144

    Google Scholar 

  • Schatten G, Schatten H (1987) Cytoskeletal alterations and nuclear architectural changes during mammalian development). Academic Press, San Diego, pp 23–54

    Google Scholar 

  • Schüpbach T (1987) Germline and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49:699–707

    Google Scholar 

  • Schüpbach T, Wieschaus E (1986a) Germline autonomy of maternal effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113:443–448

    Google Scholar 

  • Schüpbach T, Wieschaus E (1986b) Maternal effect mutations altering the anterio-posterior pattern of the Drosophila embryo. Roux's Arch Dev Biol 195:302–317

    Google Scholar 

  • Shen J-H, Li H-R, Han X-H, Wang P (1986) Observations on fertilization in sugar beet. Acta Bot Sinica 28:251–255

    Google Scholar 

  • Sonnenblick BP (1950) The early embryology of Drosophila melanogaster. In: Demerec M (ed) The biology of Drosophila. Wiley-Interscience, New York, pp 62–167

    Google Scholar 

  • Steller H, Pirrotta V (1984) Regulated expression of genes injected into early Drosophila embryos. EMBO J 3:165–173

    Google Scholar 

  • Stephenson EC, Mahowald AP (1987) Isolation of Drosophila clones encoding maternally restricted RNAs. Dev Biol 124:1–8

    Google Scholar 

  • Thierry-Mieg D (1982) Paralog, a control mutant in Drosophila melanogaster. Genetics 100:209–237

    Google Scholar 

  • Wolfner MF (1980) Ecdysone-responsive genes of the salivary gland of Drosophila melanogaster. Ph. D. thesis, Stanford University

  • Young MW, Judd BH (1978) Nonessential sequences, genes, and the polytene chromosome bands of Drosophila melanogaster. Genetics 88:723–742

    Google Scholar 

  • Zalokar M (1976) Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Dev Biol 49:419–432

    Google Scholar 

  • Zalokar M, Audit C, Erk I (1975) Developmental defects of femalesterile mutants of Drosophila melanogaster. Dev Biol 47:419–432

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Genetics and Development, Cornell University, 14853, Ithaca, NY, USA

    Haifan Lin & Mariana F. Wolfner

Authors
  1. Haifan Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariana F. Wolfner
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by B.H. Judd

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, H., Wolfner, M.F. Cloning and analysis of fs(1) Ya, a maternal effect gene required for the initiation of Drosophila embryogenesis. Mol Gen Genet 215, 257–265 (1989). https://doi.org/10.1007/BF00339726

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00339726

Key words

Search

Navigation