mRNA Distributions in Sea Urchin Embryos

  • Robert C. Angerer
  • Kathleen J. Hughes
  • Donna V. DeLeon
  • David A. Lynn
  • Lynne M. Angerer


We have developed techniques for localization of individual mRNA species in sections of sea urchin embryos using the hybridization of radioactively labeled RNA probes to tissue sections in situ. The method yields grain densities proportional to the concentration of target mRNAs and is sufficiently sensitive to allow the localization of most moderately abundant mRNAs. The major features of the method are briefly discussed, and several examples of its use are reviewed. We show that maternal histone mRNA is largely sequestered in pronuclei of unfertilized eggs and released at nuclear membrane breakdown of first cell division. We discuss several events in differentiation of cells of the dorsal ectoderm, including expression of a cell-type specific set of messenger RNAs.


Histone Gene Histone mRNAs mRNA Distribution mRNA Strand Dorsal Ectoderm 
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  1. Angerer, L.M. and Angerer, R.C. (1981). Detection of poly(A)+ RNA in sea urchin eggs and embryos by quantitative in situ hybridization. Nuc. Acids. Res. 9:2819–2840.CrossRefGoogle Scholar
  2. Brahic, M. and Haase, A.T. (1978). Detection of viral sequences of low reiteration frequency by in situ hybridization. Proc. Natl Acad. Sci. USA 75:6125–6129.CrossRefGoogle Scholar
  3. Brandhorst, B.P. (1976). Two-dimensional gel patterns of protein synthesis before and after fertilization of sea urchin eggs. Dev. Biol. 52:310–327.CrossRefGoogle Scholar
  4. Brandhorst, B.P. (1980). Simultaneous synthesis, translation, and storage of mRNA, including histone mRNA, in sea urchin eggs. Dev. Biol. 79:139–148.CrossRefGoogle Scholar
  5. Bruskin, A., Tyner, A.L., Wells, D.E., Showman, R.M., and Klein, W.H. (1981). Developmental regulation of six mRNAs enriched in ecoderm of sea urchin embryos. Dev. Biol. 87:308–318.CrossRefGoogle Scholar
  6. Butler, E. and Chamberlin, M.J. (1982). Bacteriophage SP6-RNA polymerase I. Isolation and characterization of the enzyme. J. Biol. Chem. 257:5772–5778.Google Scholar
  7. Casey, J. and Davidson, N. (1977). Rates of formation and thermal stability of RNA:DNA and DNA:DNA duplexes at high concentrations of formamide. Nuc. Acids. Res. 4:1539–1552.CrossRefGoogle Scholar
  8. Childs, G., Maxson, R., and Kedes, L.H. (1979). Histone gene expression during sea urchin embryogenesis: isolation and characterization of early and late messenger RNAs of Strongylocentrotus purpuratus by gene-specific hybridization and template activity. Dev. Biol. 73:153–173.CrossRefGoogle Scholar
  9. Costantini, F.D., Scheller, R.H., Britten, R.J., and Davidson, E.H. (1980). Message sequences and short, repetitive sequences are interspersed in sea urchin egg poly(A)+ RNAs. Nature 287:111–117.CrossRefGoogle Scholar
  10. Crane, Jr., W.R., Durica, D.S., and Van Doren, K. (1981). Actin gene expression in developing sea urchin embryos. Mol. Cell. Biol. 1:711–720.Google Scholar
  11. Davidson, E.H. (1976). Gene Activity in Early Development. Academic Press, New York.Google Scholar
  12. Davidson, E.H., Hough-Evans, B.R., and Britten, R.J. (1982). Molecular biology of the sea urchin embryo. Sci. 217:17–26.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. Ernst, S.G., Hough-Evans, B.R., Britten, R.J., and Davidson, E.H. (1980). Limited complexity of the RNA in micromeres of 16-cell sea urchin embryos. Dev. Biol. 79:119–127.CrossRefGoogle Scholar
  15. Flytzanis, C.N., Brandhorst, B.P., Britten, R.J., and Davidson, E.H. (1982). Developmental patterns of cytoplasmic transcript prevalence in sea urchin embryos. Dev. Biol. 91:27–35.CrossRefGoogle Scholar
  16. Galau, G.A., Klein, W.H., Davis, M.M., Wold, B.J., Britten, R.J., and Davidson, E.H. (1976). Structural gene sets active in embryos and adult tissues of the sea urchin. Cell 7:487–505.CrossRefGoogle Scholar
  17. Hayashi, S., Gillam, I.C., Delaney, A.D., and Tener, G.M. (1978). Acetylation of chromosome squashes of Drosophila melanogaster decreases the background in autoradiographs from hybridization with 125-labeled RNA. J. Histochem. Cytochem. 36:677–679.CrossRefGoogle Scholar
  18. Hentschel, C.C. and Birnstiel, M.L. (1981). The organization and expression of histone gene families. Cell 25:301–313.CrossRefGoogle Scholar
  19. Hieter, P.A., Hendricks, M.B., Hemminki, K., and Weinberg, E.S. (1979). Histone gene switch in the sea urchin embryo. Identification of late embryonic histone messenger ribonucleic acids and the control of their synthesis. Biochemistry 18: 2707–2716.CrossRefGoogle Scholar
  20. Hough-Evans, B.R., Wold, B.J., Ernst, S.G., Britten, R.J., and Davidson, E.H. (1977). Appearance and persistence of maternal RNA sequences in sea urchin development. Dev. Biol. 60:258–277.CrossRefGoogle Scholar
  21. Hynes, R.O. and Gross, P.R. (1970). A method for separating cells from early sea urchin embryos. Dev. Biol. 21:383–402.Google Scholar
  22. Kedes, L.H. (1979). Histone genes and histone messengers. Ann. Rev. Biochem. 48:837–870.CrossRefGoogle Scholar
  23. Lederman, L., Kawasaki, E.S., and Szabo, P. (1981). The rate of nucleic acid annealing to cytological preparations is increased in the presence of dextran sulfate. Anal. Biochem. 117:158–163.CrossRefGoogle Scholar
  24. Lynn, D.A., Angerer, L.M., Bruskin, A.M., Klein, W.H., and Angerer, R.C. (1983). Localization of a family of mRNAs to a single cell type and its precursors in developing sea urchin embryos. Proc. Natl. Acad. Sci. USA, in press.Google Scholar
  25. Mauron, A., Levy, S., Childs, G., and Kedes, L.H. (1981). Monocistronic transcription is the physiological mechanism of sea urchin embryonic histone gene expression. Mol. Cell Biol. 1:661–671.Google Scholar
  26. Mauron, A., Kedes, L.H., Hough-Evans, B.R., and Davidson, E.H. (1982). Accumulation of individual histone mRNAs during embryogenesis of the sea urchin Strongylocentrotus purpuratus. Dev. Biol. 94:425–434.CrossRefGoogle Scholar
  27. Maxson, R.E. and Wilt, F.H. (1981). The rate of histone mRNA synthesis during early sea urchin development. Dev. Biol. 83:380–386.CrossRefGoogle Scholar
  28. McClay, D.R. and Marchase, R.B. (1979). Separation of ectoderm and endoderm from sea urchin pluteus larvae and demonstration of germ layer-specific antigens. Dev. Biol. 71:289–296.CrossRefGoogle Scholar
  29. Newrock, K.M., Cohen, L.H., Hendricks, M.B., Donnelly, R.F., and Weinberg, E.S. (1978). Stage-specific mRNAs coding for subtypes of H2A and H2B histones in the sea urchin embryo. Cell 14:327–336.CrossRefGoogle Scholar
  30. Overton, C. and Weinberg, E.S. (1978). Length and sequence heterogeneity of the histone gene repeat unit of the sea urchin, S. purpuratus. Cell 14:247–258.CrossRefGoogle Scholar
  31. Rodgers, W.H. and Gross, P.R. (1978). Inhomogeneous distribution of egg RNA sequences in the early embryo. Cell 14:279–288.CrossRefGoogle Scholar
  32. Rogers, A.W. (1979). Techniques in Autoradiography. Elsevier/North Holland Biomedical Press, p. 143.Google Scholar
  33. Scheller, R.H., McAllister, L.B., Crain, Jr., W.R., Durica, D.S., Posakony, J.W., Thomas, T.L., Britten, R.J., and Davidson, E.H. (1981). Organization and expression of multiple actin genes in the sea urchin. Mol. Cell Biol. 1:609–628.Google Scholar
  34. Showman, R.M., Wells, D.E., Anstrom, J., Hursh, D.A., and Raff, R.A. (1982). Message-specific sequestration of maternal histone mRNA in the sea urchin egg. Proc. Natl. Acad. Sci. USA 79:5944–5947.CrossRefGoogle Scholar
  35. Skoultchi, A. and Gross, P.R. (1973). Maternal histone messenger RNA: Detection by molecular hybridization. Proc. Natl. Acad. Sci. USA 70:2840–2844.CrossRefGoogle Scholar
  36. Tufaro, F. and Brandhorst, B.P. (1979). Similarity of proteins synthesized by isolated blastomeres of early sea urchin embryos. Dev. Biol. 72:390–397.CrossRefGoogle Scholar
  37. Venezky, D.L., Angerer, L.M., and Angerer, R.C. (1981). Accumulation of histone repeat transcripts in the sea urchin egg pronucleus. Cell 24:385–391.CrossRefGoogle Scholar
  38. Wells, D.E., Showman, R.M., Klein, W.H., and Raff, R.A. (1981). Delayed recruitment of maternal mRNA in sea urchin embryos. Nature 292:477–478.CrossRefGoogle Scholar
  39. Wetmur, J.G. and Davidson, N. (1968). Kinetics of renaturation of DNA. J. Mol. Biol. 31:349–379.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Robert C. Angerer
    • 1
  • Kathleen J. Hughes
    • 1
  • Donna V. DeLeon
    • 1
  • David A. Lynn
    • 1
  • Lynne M. Angerer
    • 1
  1. 1.Department of BiologyUniversity of RochesterRochesterUSA

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