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RNA Synthesis and Storage During Insect Oogenesis

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Book cover Oogenesis

Part of the book series: Developmental Biology ((DEBO,volume 1))

Abstract

At fertilization, insect embryos contain large amounts of RNA in the form of transfer RNA and ribosomes to support protein synthesis, in addition to the mRNA necessary to program this activity (see review by Berry, 1982, for specific examples). The exclusive transcription of these RNAs on the maternal—rather than the zygote—genome is evident from several diverse types of experiments. Inhibitors of nucleic acid synthesis have very little effect on pregastrulation development. The necessary role of protein synthesis during these same stages is apparent from the extreme sensitivity of embryos to inhibitors of protein synthesis (Lockshin, 1966). Incorporation of amino acids into proteins during cleavage can be demonstrated to be extensive, while little incorporation of nucleotides into RNA can be observed (Fig. 1).

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References

  • Anderson, K. V., and Lengyel, J. A., 1981, Changing rates of DNA and RNA synthesis in Drosophila embryos, Dev. Biol. 82:127–138.

    Article  PubMed  CAS  Google Scholar 

  • Berry, S. J., 1982, Maternal direction of oogenesis and early embryogenesis in insects, Annu. Bev. Entomol. 267:205–227.

    Article  Google Scholar 

  • Berry, S. J., 1985, Insect nucleic acids, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 10 (G. A. Kerkut and L. I. Gilbert, eds.), Pergamon Press, Oxford (in press).

    Google Scholar 

  • Bier, K., 1963, Synthese, interzellularer transport, und abbau von ribonucleinsaure im ovar der Stubenfliege Musca domestica, J. Cell Biol. 16:436–440.

    Article  CAS  Google Scholar 

  • Brown, E. H., and King, R. C., 1964, Studies on the events resulting in the formation of an egg chamber in Drosophila melanogaster, Growth 28:41–81.

    CAS  Google Scholar 

  • Caldwell, D. G., and Emerson, C. F., 1982, Methylation of 5′ terminal caps is activated following fertilization of sea urchin eggs, Forty-first Symposium of the Society for Developmental Biology (abst).

    Google Scholar 

  • Capco, D., and Jeffery, W., 1979, Origin and spatial distribution of maternal messenger RNA during oogenesis of an insect, Oncopeltus fasciatus, J. Cell Sci. 39:63–76.

    CAS  Google Scholar 

  • Carpenter, A. T. C., 1975, Electron microscopy of meiosis in Drosophila meianogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wildtype, Chromosoma 51:157–182.

    Article  PubMed  CAS  Google Scholar 

  • Cave, M. D., 1973, Synthesis and characterization of amplified DNA oocytes of the house cricket, Acheta domesticus (Orthoptera: Gyrillaidae), Chromosoma 42:1–22.

    Article  PubMed  CAS  Google Scholar 

  • Cave, M. D., 1975, Absence of ribosomal DNA amplification in the meroistic (telotrophic) ovary of the large milkweed bug Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae), J. Cell Biol. 66:401–469.

    Article  Google Scholar 

  • Cave, M. D., 1978, Absence of amplification of ribosomal DNA in the polytrophic meroistic ovary of the giant silkmoth, Antheraea pernyi, Wilhelm Roux Arch. Dev. Biol. 184:135–142.

    Article  CAS  Google Scholar 

  • Cave, M. D., 1982, Morphological manifestations of ribosomal DNA amplification during insect oogenesis, in: Insect Ultrastructure, Vol. 1 (R. C. King and H. Akai, eds.), pp. 86–117, Plenum Press, New York.

    Google Scholar 

  • Cave, M. D., and Sixby, J., 1976, Absence of ribosomal DNA amplification in a meroistic polytrophic ovary, Exp. Cell Bes. 101:23–30.

    Article  CAS  Google Scholar 

  • Choi, W. C., and Nagl, W., 1977, Patterns of DNA and RNA synthesis during the development of ovarian nurse cells in Gerris najas (heteroptera), Dev. Biol. 61:262–272.

    Article  PubMed  CAS  Google Scholar 

  • Chooi, W. Y., 1976, RNA transcription and ribosomal protein assembly in Drosophila mela-nogaster, in: Handbook of Genetics, Vol. 5: Molecular Genetics (R. C. King, ed.), pp. 219–265, Plenum Press, New York.

    Chapter  Google Scholar 

  • Davenport, D., 1976, Transport of ribosomal RNA into the oocytes of the milkweed bug, Oncopeltus fasciatus, J. Insect Physiol. 22:925–926.

    Article  CAS  Google Scholar 

  • Davidson, E. H., 1976, Gene Action in Early Development, 2nd ed., Academic Press, New York.

    Google Scholar 

  • DeLoof, A., 1983, The meroistic insect ovary as a miniature electrophoresis chamber, Comp. Biochem. Physiol 74A:3–9.

    Article  Google Scholar 

  • Diaz, M. O., Barsacchi-Pilone, G., Mahon, K. A., and Gall, J. G., 1981, Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the Newt Notophthalmus, Cell 24:649–659.

    Article  PubMed  CAS  Google Scholar 

  • Dittmann, F., Ehni, R., and Engels, W., 1981, Bioelectric aspects of the hemipteran telotrophic ovariole. (Dysdercus intermedius), Wilhelm Roux Arch. 190:221–225.

    Article  Google Scholar 

  • Filipowicz, W., 1978, Functions of the 5′-terminal M7G cap in eukaryotic mRNA, FEBS Lett. 96:1–11.

    Article  PubMed  CAS  Google Scholar 

  • Ford, P. J., and Southern E. M., 1973, Different sequences for 5S RNA in kidney cells and ovaries of Xenopus laevis, Nature New Biol. 241:7–12.

    PubMed  CAS  Google Scholar 

  • Gall, J. G., MacGregor, H. C., and Kidston, M. E., 1969, Gene amplification in the oocytes of Dytiscid water beetles, Chromosoma 26:169–187.

    Article  PubMed  CAS  Google Scholar 

  • Gerhart, J. G., 1980, Mechanisms regulating pattern formation in the amphibian egg and early embryo, in: Biological Regulation and Development, Vol. 2 (R. F. Goldberger, ed.), pp. 133–315, Plenum Press, New York.

    Google Scholar 

  • Giardina, A., 1901, Origine dell’oöcite e delle cellule nutrici nei Dytiscus, Int. Mschr. Anat. Physiol. 18:417–484.

    Google Scholar 

  • Hall, T. J., and Cummings, M. R., 1975, In vitro synthesis and processing of ribosomal RNA in the housefly ovary, Dev. Biol. 46:233–242.

    Article  PubMed  CAS  Google Scholar 

  • Harris, S. E., and Forrest, H. S., 1967, RNA and DNA synthesis in developing eggs of the milkweed bug Oncopeltus fasciatus (Dallas), Science 156:1613–1615.

    Article  PubMed  CAS  Google Scholar 

  • Hough-Evans, B. R., Jacobs-Lorena, M., Cummings, M. R., Britten, R. J., and Davidson, E. H., 1980, Complexity of RNA in eggs of Drosophila melanogaster and Musca domestica, Genetics 95:81–94.

    PubMed  CAS  Google Scholar 

  • Huebner, E., 1981, Oocyte-follicle cell interaction during normal oogenesis and atresia in an insect, J. Ultrastruct. Res. 74:95–104.

    Article  PubMed  CAS  Google Scholar 

  • Huebner, E., 1984, The ultrastructure and development of the telotrophic ovary, in: Insect Ultrastructure, Vol. 2 (R. C. King and H. Akai, eds.), Plenum Press, New York (in press).

    Google Scholar 

  • Hughes, M., and Berry, S. J., 1970, The synthesis and secretion of ribosomes by nurse cells of Antheraea polyphemus, Dev. Biol. 23:651–664.

    Article  PubMed  CAS  Google Scholar 

  • Jäckie, H., 1980a, Two-dimensional gel analysis after removal of major proteins reveals stagedependent proteins in early insect development, FEBS Lett. 118:191–194.

    Article  Google Scholar 

  • Jäckie, H., 1980b, Actin messenger in maternal RNP particles from an insect embryo (Smittia spec, Chironomidae, Diptera), Wilhelm Roux Arch. Entw Mech. 188:225–233.

    Article  Google Scholar 

  • Jäckie, H., and Kalthoff, K., 1978, Photoreactivation of RNA in UV-irradiated insect eggs (Smittia sp., Chironomidae, Diptera). I. Photosensitized production and light-dependent disappearance of pyrimidine dimers, Photochem. Photohiol. 27:309–315.

    Article  Google Scholar 

  • Jäckie, H., and Kalthoff, K., 1980, Photoreversible UV-inactivation of messenger RNA in an insect embryo (Smittia spec. Chironomidae, Diptera), Photochem. Photohiol. 32:749–761.

    Article  Google Scholar 

  • Jacobs-Lorena, M., Hough-Evans, B. R., Britten, R. J., and Davidson, E. H., 1980, Complexity of RNA in developing oocytes of Drosophila melanogaster, Dev. Biol. 76:509–513.

    Article  PubMed  CAS  Google Scholar 

  • Jaffe, L. F., 1969, On the centripetal course of development, the Fucus egg, and self-electrophoresis, Dev. Biol. Suppl. 3:83–111.

    Google Scholar 

  • Jaffe, L. F., and Nuccitelli, R., 1974, An ultrasensitive vibrating probe for measuring steady extracellular currents, J. Cell Biol. 63:614–628.

    Article  PubMed  CAS  Google Scholar 

  • Jaffe, L. F., and Woodruff, R. I., 1979, Large electrical currents traverse developing cecropia follicles, Proc. Natl. Acad. Sci. USA 76:1328–1332.

    Article  CAS  Google Scholar 

  • Kalthoff, K., and Jäckie, H., 1982, Photoreactivation of pyrimidine dimers generated by a photosensitized reaction in RNA in insect embryos (Smittia spec), in: Trends in Photohiology (C. Helene, M. Chariler, T. H. Montenay-Garestier, and G. Laustriat, eds.), pp. 173–188, Plenum, New York.

    Chapter  Google Scholar 

  • Kalthoff, K., Kandler-Singer, I., Schmidt, O., and Zissler, D., 1975, Mitochondria and polarity in the egg of Smittia spec. (Diptera, Chironomidae): UV irradiation, respiration measurements ATP determinations and application of inhibitors, Wilhelm Roux Arch. Entw Mech. 178:99–121.

    Article  Google Scholar 

  • Kalthoff, K., Urban, K., and Jäckie, H., 1978, Photoreactivation of RNA in UV-irradiated insect eggs (Smittia sp., Chironomidae, Diptera). II. Evidence for heterogeneous light-dependent repair activities, Photochem. Photohiol. 27:317–322.

    Article  CAS  Google Scholar 

  • Kalthoff, K., Rau, K., and Edmond, J. C., 1982, Modifying effects of ultraviolet irradiation of the development of abnormal body patterns in centrifuged insect embryos (Smittia sp. Chironomidae, diptera), Dev. Biol. 91:413–422.

    Article  PubMed  CAS  Google Scholar 

  • Kandler-Singer, I., and Kalthoff, K., 1976, RNase sensitivity of an anterior morphogenetic determinant in an insect egg (Smittia spec, Chironomidae, Diptera), Proc. Natl. Acad. Sci. USA 73:3739–3743.

    Article  PubMed  CAS  Google Scholar 

  • Kastern, W. H., and Berry, S. J., 1976, Non-methylated guanosine as the 5′ terminus of capped mRNA from insect oocytes, Biochem. Biophys. Res. Commun. 71:37–44.

    Article  PubMed  CAS  Google Scholar 

  • Kastern, W. H., Underberg, D. A., and Berry, S. J., 1981, DNA-dependent RNA polymerases I and II in insect oocytes, Dev. Biol. 87:383–389.

    Article  PubMed  CAS  Google Scholar 

  • Kastern, W. H., Swindlehurst, M., Aaron, C., Hooper, J., and Berry, S. J., 1982, Control of mRNA translation in oocytes and developing embryos of giant moths. 1. Function of the 5′ terminal “cap” in the tobacco hornworm, Manduca sexta, Dev. Biol. 89:437–449.

    Article  CAS  Google Scholar 

  • King, R. C., 1970, Ovarian Development in Drosophila melanogaster, 227, Academic Press, New York and London.

    Google Scholar 

  • King, R. C., and Aggarwal S. K., 1965, Oogenesis in Hyalophora cecropia, Growth 29:17–83.

    PubMed  CAS  Google Scholar 

  • King, R. C., and Büning, J., 1985, The origin and functioning of insects oocytes and nurse cells, in: Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 1 (G. A. Kerkut and L. I. Gilbert, eds.), Pergamon Press, Oxford (in press).

    Google Scholar 

  • King, R. C., Aggarwal, S. K., and Aggarwal, U., 1968, The development of the female Drosophila reproductive system, J. Morphol. 124:143–166.

    Article  PubMed  CAS  Google Scholar 

  • King, R. C., Cassidy, J. D., and Rousset, A., 1982, The formation of clones of interconnected cells during gametogenesis in insects, in: Insect Ultrastructure, Vol. 1 (R. C. King and H. Akai, eds.), pp. 3–31, Plenum Press, New York.

    Google Scholar 

  • Koch, E. A., and King, R. C., 1969, Further studies on the ring canal system of the ovarian cystocytes of Drosophila melanogaster, Z. Zellforsch. 102:129–152.

    Article  PubMed  CAS  Google Scholar 

  • Lamb, M. M., and Laird, C. D., 1976, The size of Poly(A)-containing RNAs in Drosophila melanogaster embryos, Biochem. Genet. 14:357–371.

    Article  PubMed  CAS  Google Scholar 

  • Lima-de-Faria, A., Birnstiel, M., and Jaworska, H., 1969, Amplication of ribosomal cistrons in the heterochromatin of Acheta, Genetics Suppl 1 61:145–159.

    CAS  Google Scholar 

  • Limbourg, B., and Zalokar, M., 1973, Permeabilization of Drosophila eggs, Dev. Biol. 35:382–387.

    Article  PubMed  CAS  Google Scholar 

  • Lockshin, R. A., 1966, Insect embryogenesis: Macromolecular synthesis during early development, Science 154:775–776.

    Article  PubMed  CAS  Google Scholar 

  • Long, E. O., and Dawid, I. B., 1980, Repeated genes in eukaryotes, Annu. Rev. Biochem. 49:727–764.

    Article  PubMed  CAS  Google Scholar 

  • Mahowald, A. P., and Strassheim, J. M., 1970, Intracellular migration of centrioles in the germarium of Drosophila melanogaster, J. Cell Biol. 45:306–320.

    Article  PubMed  CAS  Google Scholar 

  • Meinhardt, H., 1977, A model for pattern formation in insect embryogenesis,J. Cell Sci. 23:117–139.

    Google Scholar 

  • Mermod, J. J., Schatz, G., and Crippa, M., 1980, Specific control of messenger translation in Drosophila oocytes and embryos, Dev. Biol. 75:177–186.

    Article  PubMed  CAS  Google Scholar 

  • Miller, O. L., and Beatty, B. R., 1969, Visualization of nucleolar genes, Science 164:955–957.

    Article  PubMed  Google Scholar 

  • Moon, R. T., Danilchik, M. V., and Hille, M. B., 1982, An assessment of the masked message hypothesis: Sea urchin messenger ribonucleoprotein complexes are efficient templates for in vitro protein synthesis, Dev. Biol. 93:389–403.

    Article  PubMed  CAS  Google Scholar 

  • Moon, R. T., Nicosia, R. F., Olsen, C., Hille, M. B., and Jeffery, W. R., 1983, The cytoskeletal framework of sea urchin eggs and embryos: Developmental changes in the association of messenger RNA, Dev. Biol. 95:447–458.

    Article  PubMed  CAS  Google Scholar 

  • Muhlach, W. L., and Schwalm, F. E., 1977, Utilization of uridine in developing ovarioles of the kelp fly, Coelopa, J. Insect Physiol. 23:931–937.

    Article  CAS  Google Scholar 

  • Newport, J., and Kirschner, M., 1982a, A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage, Cell 30:675–686.

    Article  PubMed  CAS  Google Scholar 

  • Newport, J., and Kirschner, M., 1982b, A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription, Cell 30:687–696.

    Article  PubMed  CAS  Google Scholar 

  • Paglia, L. M., Berry, S. J., and Kastern, W. H., 1976a, Messenger RNA synthesis, transport, and storage in silkmoth ovarian follicles, Dev. Biol. 51:173–181.

    Article  PubMed  CAS  Google Scholar 

  • Paglia, L. M., Kastern, W. H., and Berry, S. J., 1976b, Messenger ribonucleoprotein particles in silkmoth oogenesis, Dev. Biol. 51:182–189.

    Article  PubMed  CAS  Google Scholar 

  • Pietruschka, F., and Bier, K., 1972, Autoradiographische Untersuchungen zur RNS-und Protein-Synthese in der fruhen Embryogenese von Musca domestica, Wilhelm Roux Arch. Entw Mech. 169:56–69.

    Article  Google Scholar 

  • Pollak, S. B., and Telfer, W. H., 1969, RNA in cecropia moth ovaries: Sites of synthesis, transport, and storage,J. Exp. Zool. 170:1–24.

    Article  Google Scholar 

  • Raff, R., 1980, Masked messenger RNA and the regulation of protein synthesis in eggs and embryos, in: Cell Biology, Vol. 4 (D. M. Prescott, ed.), pp. 107–136, Academic Press, New York.

    Google Scholar 

  • Renkawitz, R., and Kunz, W., 1975, Independent replication of the ribosomal RNA genes in the polytrophic-meroistic ovaries of Calliphora erythrocephala, Drosophila hydei, and Sarcophaga barbata, Chromosoma 53:131–140.

    Article  PubMed  CAS  Google Scholar 

  • Spear, B. B., and Gall, J. G., 1974, Independent control of ribosomal gene replication in poly-tene chromosomes of D. melanogaster, Proc Natl Acad. Sci. USA 70:1359–1363.

    Article  Google Scholar 

  • Struhl, G., 1981, A gene product required for correct initiation of segmental determination in Drosophila, Nature 293:36–41.

    CAS  Google Scholar 

  • Telfer, W. H., 1975, Development and physiology of the oocyte-nurse cell synctium, Adv. Insect Physiol. 11:223–320.

    Article  Google Scholar 

  • Telfer, W. H., Woodruff, R. I., and Huebner E., 1981, Electrical polarity and cellular differentiation in meroistic ovaries, Am. Zool. 21:675–686.

    Google Scholar 

  • Winter, H., 1974, Ribonucleoprotein-partikel aus dem telotroph-meroistischen Ovar von Dyserrcus intermedius Dis. (Heteroptera, Pyrrhoc.) und ihr Verhalten im zellfreien Proteinsynthesesystem, Wilhelm Roux Arch. Entw Mech. 175:103–127.

    Article  CAS  Google Scholar 

  • Wollberg, Z., Cohen, E., and Kalina, M., 1976, Electrical properties of developing oocytes of the migratory locust, Locusta migratoria, J. Cell Physiol. 88:145–158.

    Article  CAS  Google Scholar 

  • Woodruff, R. I., and Telfer, W. H., 1973, Polarized intercellular bridges in the ovarian follicles of the Cecropia moth,J. Cell Biol. 58:172–188.

    Article  PubMed  CAS  Google Scholar 

  • Woodruff, R. I., and Telfer, W. H., 1980, Electrophoresis of proteins in intercellular bridges, Nature 286:84–86.

    Article  PubMed  CAS  Google Scholar 

  • Zalokar, M., 1976, Autoradiographic study of protein and RNA formation during early development of Drosophila eggs, Dev. Biol. 49:425–437.

    Article  PubMed  CAS  Google Scholar 

  • Zissler, D., and Sander, K., 1982, The cytoplasmic architecture of the insect egg cell, in: Insect Ultrastructure, Vol. 1 (R. C. King and H. Akai, eds.), pp. 189–221, Plenum Press, New York.

    Google Scholar 

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  1. Department of Biology, Hall-Atwater and Shanklin Laboratories, Wesleyan University, Middletown, Connecticut, 06457, USA

    Spencer J. Berry

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  1. Spencer J. Berry
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  1. University of Calgary, Calgary, Alberta, Canada

    Leon W. Browder

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© 1985 Plenum Press, New York

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Berry, S.J. (1985). RNA Synthesis and Storage During Insect Oogenesis. In: Browder, L.W. (eds) Oogenesis. Developmental Biology, vol 1. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6814-8_8

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  • DOI: https://doi.org/10.1007/978-1-4615-6814-8_8

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