Skip to main content

Localization of polyadenylated RNAs during teloplasm formation and cleavage in leech embryos

Roux's archives of developmental biology volume 204, pages 46–53 (1994)Cite this article

Abstract

In the embryos of glossiphoniid leeches, as in many annelids, cytoplasmic reorganization prior to first cleavage generates domains of yolk-deficient cytoplasm (called teloplasm) that are sequestered during the first three cell divisions to the D' macromere. Subsequently, the D' macromere generates a set of embryonic stem cells (teloblasts) that are the progenitors of the definitive segmental tissues. The hypothesis that fate-determining substances are localized within the teloplasm and segregated to the D′ macromere during cleavage is supported by experiments in which a redistribution of yolk-defcient cytoplasm changes the fate of blastomeres that inherit it (Astrow et al. 1987; Devries 1973; Nelson and Weisblat 1992). As a step toward identifying fate-determining factors in teloplasm, we describe the distribution of polyadenylated RNAs (polyA+ RNA) in the early embryo of the leech,Helobdella triserialis, as inferred from in situ hybridization using tritiated polyuridylic acid (3H-polyU). Our results indicate that polyA+ RNA colocalizes with teloplasm during cytoplasmic rearrangements resulting in teloplasm formation, and that it remains concentrated in the teloplasm during the cell divisions and a second cytoplasmic rearrangement during early embryogenesis. Lesser amounts of polyA+ RNA appear to be localized in cortical cytoplasm at most stages.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Anderson DL (1975) Embryology and pylogeny in annelids and arthropods. Pergamon Press, Oxford

    Google Scholar 

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

    Google Scholar 

  • Astrow SH, Holton B, Weisblat DA (1987) Centrifugation redistributes factors determining cleavage patterns in leech embryos. Dev. Biol. 120:270–283

    Google Scholar 

  • Astrow SH, Holton B, Weisblat DA (1989) Teloplasm formation in a leechHelobdella triserialis, is a microtubule-dependent process. Dev Biol 135:306–319

    Google Scholar 

  • Berleth T, Burri M, Thomas G, Bopp D, Richstein S, Frigerio G, Noll M, Nusslein-Volhard C (1988) The role of localization ofbiocid RNA in organizing the anterior pattern of theDrosophila embryo. EMBO J 7:1749–1756

    Google Scholar 

  • Bishop JO, M Rosbash, Evans D (1974) Polynucleotide sequences in eukaryotic DNA and RNA that form ribonuclease-resistant complexes with polyuridylic acid. J Mol Biol 85:75–86

    Google Scholar 

  • Bissen ST, Weisblat DA (1989) The durations and compositions of cell cycles in embryos of the leech,Helobdella triserialis. Development 106:105–118

    Google Scholar 

  • Bissen ST, Weisblat DA (1991) Transcription in leech: mRNA synthesis is required for early cleavages inHelobdella embryos. Dev Biol 146:12–23

    Google Scholar 

  • Brandhorst BP, McConkey EH (1974) Stability of nuclear RNA in mammalian cells. J Mol Biol 85:451–563

    Google Scholar 

  • Capco DG, Jeffery WR (1978) Differential distribution of poly (A)-containing RNA in the embryonic cells ofOncopeltus fasciatus. Dev Biol 67:137–151

    Google Scholar 

  • Clegg KB, Piko L (1983) Poly(A) length, cytoplasmic adenylation and synthesis of poly(A)+ RNA in early mouse embryos. Dev Biol 95:331–341

    Google Scholar 

  • Davidson E (1986) Gene activity in early development. Academic Press, New York

    Google Scholar 

  • Devries J (1973) Aspect du déterminisme embryonnaire an cours des premiers stades de la segmentation chez le combricienEisenia foetida. Annales d'Embryologie et de Morphogénèse 6:95–108

    Google Scholar 

  • Driever W, Nüsslein-Volhard C (1988a) A gradient ofbiocid protein inDrosophila embryos. Cell 54:83–93

    Google Scholar 

  • Driever W, Nüsslein-Volhard C (1988b) Thebiocid protein determines position in theDrosophiola embryo in a concentration dependent manner. Cell 54:95–104

    Google Scholar 

  • Fernandez J (1980) Embryonic development of the glossiphoniid leechTheromyzon rude: characterization of developmental stages. Dev Biol 76:245–262

    Google Scholar 

  • Fernandez J, Olea N (1982) Embryonic development of glossiphoniid leeches. In: Harrison FW, Cowden RR (eds) Developmental biology of freshwater invertebrates. A R Liss, New York, pp 317–362

    Google Scholar 

  • Fernandez J, Olea N, Matte C (1987) Structure and development of the egg of the glossiphoniid leechTheramyzon rude: characterization of developmental stages and structure of the early uncleaved egg. Development 100:211–226

    Google Scholar 

  • Fernandez J, Stent GS (1980) Embryonic development of the glossiphoniid leechTheromyzon rude: structure and development of the germinal bands. Dev Biol 78:407–434

    Google Scholar 

  • Holton B, Astrow SH, Wesiblat DA (1989) Animal and vegetal teloplasms mix in the early embryo of the leech,Helobdella triserialis. Dev Biol 131:182–188

    Google Scholar 

  • Jeffery WJ (1983) Messenger RNA localization and cytoskeletal domains in ascidian embryos. In: Jeffery WR, Raff RA (eds) Time, space and pattern in embryonic development. AR Liss, New York, pp 241–259

    Google Scholar 

  • Jeffery WJ, Meier S (1983) A yellow crescent cytoskeletal domain in ascidian eggs and its role in early development. Dev Biol 96:125–143

    Google Scholar 

  • Kalthoff K (1983) Cytoplasmic determinants in dipteran eggs. In: Jeffery WR, Raff RA (eds) Time, space and pattern in embryonic development. AR Liss, New York, pp 313–348

    Google Scholar 

  • Kostriken R, Weisblat DA (1992) Dynamic expression of aWnt gene in embryonic epithelium of the leech. Dev Biol 151:225–241

    Google Scholar 

  • Mahoney PA, Lengyel JA (1987) The zygotic segmentation mutanttailless alters the blastoderm fate map of theDrosophila embryo. Dev Biol 122:464–470

    Google Scholar 

  • Melton DA (1987) Translocation of a localized maternal mRNA to the vegetal pole ofXenopus oocytes. Nature 328:80–82

    Google Scholar 

  • Nardelli-Haefliger D, Shankland M (1993)Lox10, a member of theNK-2 homeobox gene class, is expressed in a segmental pattern in the endoderm and in the cephalic nervous system of the leechHelobbdella. Development 118:877–892

    Google Scholar 

  • Nelson BH, Weisblat DA (1991) Conversion of ectoderm to mesoderm by cytoplasmic extrusion in leech embryos. Science 253:435–438

    Google Scholar 

  • Nelson BH, Weisblat DA (1992) Cytoplasmic and cortical determinants interact to specify ectoderm and mesoderm in the leech embryo. Development 115:103–115

    Google Scholar 

  • Sanding M, Dohle W (1988) The cleavage pattern in the leechTheromyzon tessulatum (Hirudinea, Glossiphoniidae). J Morphol 196:217–252

    Google Scholar 

  • Schleip W (1914) Die Entwicklung zentrifugiertier Eier vonClepsine sexolculata. Zool Jahrb AN Anat Ontog Tiere 37:236–253

    Google Scholar 

  • Schimizu T (1982) Ooplasmic segregation in theTubifex egg: mode of pole plasm accumulation and possible involvement of microfilaments. Roux's Arch Dev Biol 191:246–256

    Google Scholar 

  • Shimizu T (1984) Dynamics of the actin microfilament system in theTubifex during ooplasmic segregation. Dev Biol 106:414–426

    Google Scholar 

  • Shimizu T (1986) Bipolar segregation of mitochondria, actin network, and surface in theTubifex egg: Role of cortical polarity. Dev Biol 116:241–251

    Google Scholar 

  • Shimizu T (1989) Asymmetric segregation and polarized redistribution of pole plasm during early cleavages in theTubifex embryo: role of actin networks and mitotic apparatus. Dev Growth Differ 31:283–297

    Google Scholar 

  • Stent GS, Kristan WB Jr, Torrence SA, French KA, Weisblat DA (1992) Development of the leech nervous system. Int Rev Neurobiol 33:109–193

    Google Scholar 

  • Weisblat DA, Zackson SL, Blair SS, Young JD (1980) Cell lineage analysis by intracellular injection of fluorescent tracers. Science 209:1538–1541

    Google Scholar 

  • Weisblat DA, Kim SY, Stent GS (1984) Embryonic origins of cells in the leechHelobdella triserialis. Dev Biol 104:65–85

    Google Scholar 

  • Weisblat DA, Shankland M (1985) Cell lineage and segmentation in the leech. Phil Trans R Soc 312:39–56

    Google Scholar 

  • Whitman CO (1978) The embryology ofClepsine. Quart J Microscop Sci 18:215–315

    Google Scholar 

  • Wilson EB (1925) The cell in development and heredity. Macmillan, New York

    Google Scholar 

  • Wilt FH (1973) Polyadenylation of maternal RNA of sea urchin eggs after fertilization. Proc Natl Acad Sci USA 70:2345–2349

    Google Scholar 

Download references

Author information

Affiliations

  1. Department of Molecular and Cell Biology, University of California, 385 LSA, 94720, Berkeley, CA, USA

    David A. Weisblat

  2. Department of Biology and Microbiology, University of Wisconsin, 54901, Oshkosh, WI, USA

    Beatrice Holton

  3. Department of Cell Biology and Anatomy, New York Medical College, 10595, Valhalla, NY, USA

    Cathy J. Wedeen

  4. Department of Biological Sciences, University of Southern California, 90089, Los Angeles, CA, USA

    Stephanie H. Astrow

Authors
  1. Beatrice Holton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cathy J. Wedeen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephanie H. Astrow
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David A. Weisblat
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Holton, B., Wedeen, C.J., Astrow, S.H. et al. Localization of polyadenylated RNAs during teloplasm formation and cleavage in leech embryos. Roux's Arch Dev Biol 204, 46–53 (1994). https://doi.org/10.1007/BF00744872

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00744872

Key words

  • Leech
  • Annelid
  • Maternal RNA