Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Degradation of maternal poly(A)-containing RNA during early embryogenesis of an insect (Smittia spec., chironomidae, diptera)

  • 47 Accesses

  • 10 Citations

Summary

Eggs of the chironomid midgeSmittia spec. were shown to contain maternal rRNA, tRNA and poly(A)-containing RNA. The ribonucleoprotein spectrum consisted of monosomes, ribosomal subunits, and subribosomal particles, whereas polysomes could be detected only in small amounts. Poly(A)-containing RNA was found in different regions of the RNP spectrum, mainly between 15 S and 60 S. After labelling maternal RNA by feeding tritiated uridine to the larvae, the radioactivity associated with poly(A)-containing RNA accounted for about 4% of the label in the total RNA extracted from newly deposited eggs. About half of the radioactivity in the poly(A)-containing RNA was lost between egg deposition and an advanced blastoderm stage. The loss was accompanied by both a decrease in the size of the poly(A)-containing RNA molecules and a shift of poly(A)-containing RNP particles to less dense regions in sucrose gradients. Comparison with poly(A)-containing RNA synthesized by the embryo indicates that the reduction in size of maternal poly(A)-containing RNA is not artifactual but reflects its degradation after the formation of blastoderm.

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

References

  1. Bull, A.: Bicaudal, a genetic factor which affects the polarity of the embryo inDrosophila melanogaster. J. Exp. Zool.161, 221–241 (1966)

  2. Civelli, O., Vincent A., Buri, J.-F., Scherrer, K.: Evidence for translational inhibitor linked to globin mRNA in untranslated free cytoplasmic messenger ribonucleoprotein complexes. FEBS Lett.72, 71–76 (1976)

  3. Edström, J.E., Rydlander, H.: Identification of cytoplasmatic RNA from individualBalbiani rings. Biol. Zbl.95, 521–530 (1976).

  4. Edström, J.E., Tanguay, R.: Cytoplasmic ribonucleic acids with messenger characteristics in salivary gland cells ofChironomus tentans, J. Mol. Biol.84, 569–583 (1974)

  5. Felicetti, L., Amaldi, P., Moretti, S., Campioni, N. Urbani, C.: Intracellular distribution, sedimentation values and template activity of polyadenylic acid-containing RNA stored inArtemia salina cysts. Cell Diff4, 339–354 (1975)

  6. Franke, W. W., Krien, S., Brown, R. M. Jr.: Simultaneous glutaraldehyd-osmium tetroxide fixation with postosmication. An improved fixation procedure for electron microscopy of plant and animal cells, Histochemistry19, 1642–1647 (1969)

  7. Jäckle, H.: Untersuchungen über RNA-haltige Eikomponenten in normalen und uv-bestrahlten Eiern vonSmittia spec. (Chironomidae, Diptera). Dissertation, Universität Freiburg i. Br. (1977)

  8. Jäckle, H., Kalthoff, K.: Photoreactivation of RNA in UV-irradiated insect eggs (Smittia spec., Chironomidae, Diptera) — I. Photosensitized production and light-dependent disappearance of pyrimidine dimers. Photochem. Photobiol.27, 309–319 (1978)

  9. Kalthoff, K.: Position of targets and period of competence for UV induction of the malformation ‘double abdomen’ in the egg ofSmittia spec. (Diptera, Chironomidae). Wilhelm Roux' Arch. Entwicklungsmech. Org.169, 63–84 (1971).

  10. Kalthoff, K.: Photoreversion of UV-induction of malformation ‘double abdomen’ in the egg ofSmittia spec. (Diptera, Chironomidae): UV irradiation, respiration measurements, ATP determinationsand application of inhibitors. Wilhelm Roux' Arch. Entwicklungsmech. Org.178, 99–121 (1975)

  11. Kalthoff, K.: Specification of the antero-posterior body pattern in insect eggs. In: Insect development (P.A. Lawrence, ed.), pp. 53–75, Oxford: Blackwell 1976

  12. Kalthoff, K., Hanel, P., Zissler, D.: A morphogenetic determinant in the anterior pole of an insect egg (Smittia spec., Chironomidae, Diptera). Localization by combined centrifugation and ultraviolet irradiation. Dev. Biol.55, 285–305 (1977)

  13. Kalthoff, K., Sander, K.: Der Entwicklungsgang der Mißbildung ‘Dopple abdomen’ im partiell UV-bestrahlten Ei vonSmittia parthenogenetica (Diptera, Chironomidae) Wilhelm Roux' Arch. Entwicklungsmech. Org.161, 129–146 (1968)

  14. Kandler-Singer, I., Kalthoff, K.: RNase sensitivity of an anterior determinant in an insect egg (Smittia spec., Chironomidae, Diptera). Proc. Natl. Acad. Sci. USA73, 3739–3743 (1976)

  15. Lengyel, J., Penman, S.: HnRNA size and processing as related to different DNA content in two dipterans:Drosophila andAedes. Cell5, 281–290 (1975)

  16. Limbourg, B., Zalokar, M.: Permeabilization ofDrosophila eggs. Dev. Biol.35, 382–387 (1973)

  17. Lovett, J.A., Goldstein, E.S.: The cytoplasmic distribution and characterization of poly(A)+ RNA in oocytes and embryos ofDrosophila. Dev. Biol.61, 79–85 (1977)

  18. Mahowald, S.P.: Oogenesis. In: Developmental systems: Insects (S.J. Counce, C.H. Waddington, eds.), Vol. 1, pp. 1–47. London, New York: Academic Press 1972

  19. Mahowald, A.P., Tiefert, M.: Fine structural changes in theDrosophila oocyte nucleus during a short period of RNA synthesis. Wilhelm Roux' Arch. Entwicklungsmech. Org.165, 8–25 (1970)

  20. Mays, U.: Stofftransport im Ovar vonPyrrhocoris apterus L. Autoradiographische Untersuchungen zum Stofftransport von den Nährzellen zur Oocyte der Feuerwanze,Pyrrhocoris apterus L. (Heteroptera). Z. Zellforsch.123, 395–410 (1972)

  21. Newrock, K.M., Raff, R.A.: Polar lobe specific regulation of translation in embryos ofIlyanassa obsoleta. Dev. Biol.42, 242–261 (1975)

  22. Nüsslein-Volhard, C.: Genetic analysis of Pattern-formation in the Embryo ofDrosophila melanogaster. Characterization of the maternal-effect mutant bicaudal. Wilhelm Roux' Arch. Entwicklungsmech. Org.183, 249–268 (1977)

  23. Oullette, A.J., Kumar, A., Malt, R.A.: Physical aspects and cytoplasmic distribution of messenger RNA in mouse kidney. Biochim. Biophys. Acta425, 384–395 (1976)

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

  25. Perry, R.P.: Processing of RNA. Annu. Rev. Biochem.45, 605 (1976)

  26. Pietruschka, F., Bier, K.: Autoradiographische Untersuchungen zur RNS- und Proteinsynthese in der frühen Embryogenese vonMusca domestica. Wilhelm Roux' Arch. Entwicklungsmech. Org.169, 56–69 (1972)

  27. Rosbash, M., Ford, P.J.: Polyadenylic acid-containing RNA inXenopus laevis oocytes. J. Mol. Biol.85, 87–101 (1974)

  28. Schmidt, O., Jäckle, H.: RNA synthesized during oogenesis and early embryogenesis in an insect egg (Euscelis plebejus) Wilhelm Roux' Arch. Entwicklungsmech. Org.184, 143–153 (1978)

  29. Schnetter, W.:Zur Proteinsynthese in der frühen Embryonalentwicklung vonLeptinotarsa decemlineata. Verh. Dtsch. Zool. Ges. 197–201 (1975)

  30. Spirin, A.S.: Informosomes, Eur. J. Biochem.10, 20–35 (1969)

  31. Spradling, A., Penman, S., Pardue, M.L.: Analysis ofDrosophila mRNA byin situ hybridization: Sequences transcribed in normal and heat shocked cultured cells. Cell4, 395–404 (1975)

  32. Telfer, W.H.: Development and physiology of the oocyte nurse cell syncytium. Adv. Insect Physiol.11, 223–319 (1975)

  33. Tomkins, J.K., Billington, F.: A simple procedure for study of ribosomal and transfer RNA ofDrosophila melanogaster. Anal. Biochem.50, 494–499 (1972)

  34. Vincent, A., Civelli, O., Buri, J.-F., Scherrer, K.: Correlation of specific coding sequences with specific proteins associated in untranslated cytoplasmic messenger ribonucleoprotein complexes of Duck erythroblasts. FEBS Lett.77, 281–286 (1977)

  35. Winter, H.: Ribonucleoprotein-partikel aus dem telotroph-meroistischen ovar vonDysdercus intermedius Dist. (Heteroptera, Pyrrhoc.) und ihr Verhalten im zellfreien Proteinsynthesesystem. Wilhelm Roux' Arch. Entwicklungsmech. Org.175, 103–127 (1974)

  36. Winter, H., Wiemann-Weis, D., Duspiva, F.: Endogene Synthese kurzlebiger Messenger-RNS in der Oocyte vonDysdercus intermedius Dist. nach Abschluß der Vitellogenese. W. Roux' Arch. Entwicklungsmech. Org.182, 39–58 (1977)

  37. Yajima, H.: Studies on embryonic determination of the harlequinfly.Chironomus dorsalis. II. Effect of partial irradiation of the egg by ultraviolet light. J. Embryol. Exp. Morphol.12, 89–100 (1964)

  38. Zalokar, M.: Autoradiographic studies of protein and RNA formation during early development ofDrosophila eggs. Dev. Biol.49, 425–437 (1976)

  39. Zissler, D., Sander, K.: The cytoplasmic architecture of the egg cell ofSmittia spec. I. Anterior and posterior pole regions. Wilhelm Roux' Arch. Entwicklungsmech. Org.172, 175–186 (1973)

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Jäckle, H. Degradation of maternal poly(A)-containing RNA during early embryogenesis of an insect (Smittia spec., chironomidae, diptera). Wilhelm Roux' Archiv 187, 179–193 (1979). https://doi.org/10.1007/BF00848270

Download citation

Key words

  • Insect embryogenesis
  • Poly(A)-containing RNA
  • maternal RNA
  • RNP-particles