Advertisement

Isolation and Characterization of Genes Differentially Expressed in Early Drosophila Embryogenesis

  • Judith A. Lengyel
  • Steven R. Thomas
  • Paul David Boyer
  • Fidel Salas
  • Teresa R. Strecker
  • Inyong Lee
  • Melissa L. Graham
  • Margaret Roark
  • Eileen M. Underwood

Abstract

Important events of Drosophila embryogenesis are compressed into a remarkably short period: in the first 3.5 hours after fertilization, rapid nuclear multiplication, cellularization, activation of transcription, and the determination of much of the basic pattern of the larva and adult occur. In this chapter we review the evidence that only a relatively small number of genes are involved in controlling these processes, and that of such genes, those transcribed as part of the maternal program may provide qualitatively different information than those transcribed as part of the zygotic program. Reasoning that genes which play a major role in events specific to early embryogenesis should be expressed differentially during this time period, we have used recombinant DNA techniques to isolate members of two such classes of genes. One class encodes mRNAs which are part of the maternal population, but which disappear rapidly during embryogenesis; the other encodes mRNAs whose expression is primarily zygotic, reaching a peak at the blastoderm or late gastrula stage. We expect that genetic and biochemical analyses of these cloned sequences will provide insight into events specific to early embryogenesis.

Keywords

Early Embryogenesis Drosophila Embryo Polar Granule Maternal mRNA Blastoderm Stage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, K.V. and Lengyel, J.A. (1979). Rates of synthesis of major classes of RNA in Drosophila embryos. Devel. Biol. 70:217–231.CrossRefGoogle Scholar
  2. Anderson, K.V. and Lengyel, J.A. (1981). Changing rates of DNA and RNA synthesis in Drosophila embryos. Devel. Biol. 82:127–138.CrossRefGoogle Scholar
  3. Anderson, K.V. and Lengyel, J.A. (1983). Histone gene expression in Drosophila development: Multiple levels of gene regulation. In “Histone Genes and Histone Gene Expression,” G. Stein, J. Stein, and W. Marzluff (eds.). John Wiley and Sons, in press.Google Scholar
  4. Anderson, K.V. and Nusslein-Volhard, C. (1983). Genetic analysis of dorsal-ventral embryonic pattern in Drosophila. In “Drosophila in Pattern Formation,” G. Malacinski and S. Bryant (eds.), in press.Google Scholar
  5. Arthur, C.G., Weide, C.M., Vincent, W.S., and Goldstein, E.S. (1979). mRNA sequence diversity during early embryogenesis in Drosophila melanogaster. Exp. Cell. Res. 121:87–94.CrossRefGoogle Scholar
  6. Bakken, A.H. (1973). A cytological and genetic study of oogenesis in Drosophila melanogaster. Devel. Biol. 33:100–122.CrossRefGoogle Scholar
  7. Benoist, C., O’Hare, K.O., Breathnach, R., and Chambon, P. (1979). The ovalbumin gene-sequence of putative control regions. Nuc. Acadis Res. 8:127–142.CrossRefGoogle Scholar
  8. Benton, W.D. and Davis, R.W. (1977). Screening recombinant clones by hybridization to single plaques in situ. Science 196:180–182.CrossRefGoogle Scholar
  9. Buell, G.N., Wickens, M.P., Payvar, F., and Schmike, R.T. (1978). Synthesis of full-length cDNA from four partially purified oviduct mRNAs. J. Biol. Chem. 253:2471–2482.Google Scholar
  10. Capdevila, M.P. and Garcia-Bellido, A. (1974). Development and genetic analysis of bithorax phenocopies in Drosophila. Nature 250:500–502.CrossRefGoogle Scholar
  11. Carramolino, L., Ruiz-Gomez, M., Guerrero, M.d.C., Campuzano, S., and Modolell, J. (1982). “DNA map of mutations at the scute locus of Drosophila melanogaster.” The EMBO Journal I:1185–1191.Google Scholar
  12. Chan, L-N. and Gehring, W. (1971). Determination of blastoderm cells in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68:2217–2221.CrossRefGoogle Scholar
  13. Clarke, L. and Carbon, J. (1976). A colony bank containing synthetic ColEl hybrid plasmids representative of the entire E. coli genome. Cell 9:91–99.Google Scholar
  14. Cline, T.W. (1976). A sex-specific, temperature-sensitive maternal effect of the daughterless mutation of Drosophila melanogaster. Genetics 84:723–742.Google Scholar
  15. Cline, T.W. (1978). Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90:683–698.Google Scholar
  16. Fullilove, S.L. and Jacobson, A.G. (1978). Embryonic development: descriptive. In “The Genetics and Biology of Drosophila,” Vol 2c. M. Ashburner and T.R.F. Wright (eds.), pp. 105–227. Academic Press, New York.Google Scholar
  17. Gans, M., Audit, C., and Masson, M. (1975). Isolation and characterzation of sex-linked female sterile mutants in Drosophila melanogaster. Genetics 81: 683–704.Google Scholar
  18. Goldstein, E.S. and Arthur, C.G. (1979). Isolation and characterization of cDNA complementary to transient maternal poly(A)+ RNA from the Drosophila oocyte. Biochim. Biophys. Acta 565:265–274.Google Scholar
  19. Goldstein, E.S. and Snyder, L.A. (1973). Protein synthesis and distribution of ribosomal elements in ovarian oocytes and developmental stages of Drosophila melanogaster. Exp. Cell Res. 81:47–56.CrossRefGoogle Scholar
  20. Gutzeit, H.O. (1980). Expression of the zygotic genome in blastoderm stage embryos of Drosophila: an analysis of a specific protein. Wilhelm Roux’ Archiv. 188:153–156.CrossRefGoogle Scholar
  21. Hanahan, D. and Meselson, M. (1980). Plasmid screening at high colony density. Gene 10:63–67.CrossRefGoogle Scholar
  22. 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.Google Scholar
  23. Illmensee, K. and Mahowald, A.P. (1974). Transplantation of posterior polar plasm in Drosophila: Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA 71:1016–1020.CrossRefGoogle Scholar
  24. Illmensee, K. and Mahowald, A.P. (1976). The autonomous function of germ plasm in a somatic region of the Drosophila egg. Exp. Cell. Res. 97:127–140.CrossRefGoogle Scholar
  25. Illmensee, K., Mahowald, A.P., and Loomis, M.R. (1976). The ontogeny of germ plasm during oogenesis in Drosophila. Devel. Biol. 49:40–65.CrossRefGoogle Scholar
  26. Jackie, H. and Kalthoff, K. (1979). RNA and Protein Synthesis in Developing Embryos of Smittia spec. (Chironomidae, Diptera). Wilhelm Roux’ Archiv. 187:283–305.CrossRefGoogle Scholar
  27. Janning, W. (1978). Gynandromorph fate maps in Drosophila. In “Genetic Mosaics and Cell Differentiation,” W.J. Gehring (ed.), pp. 1–28. Springer Verlag, New York.Google Scholar
  28. Kalthoff, K. (1979). Analysis of a morphogenetic determinant in an insect embryo. In “Determinants of Spatial Organization,” I. Konigsberg and S. Subtelney (eds.), pp. 97–126. Academic Press, New York.Google Scholar
  29. King, R.C. and Mohler, D.J. (1975). The genetic analysis of oogenesis in Drosophila melanogaster. In “Handbook of Genetics,” Vol. 3, R.C. King (ed.), pp. 757–791. Plenum Publishing, New York.CrossRefGoogle Scholar
  30. Konrad, K.D., Goralski, T.J., Turner, F.R., and Mahowald, A.P. (1982). Maternal effect mutation affecting gastrulation. J. Cell Biol. 95:159a.Google Scholar
  31. Lerner, R.A. (1982). Tapping the immunological repertoire to produce antibodies of predetermined specificity. Nature 299:592–596.CrossRefGoogle Scholar
  32. Lerner, R.A., Sutcliffe, J.G., and Shinnick, T.M. (1981). Antibodies to chemically synthesized peptides predicted from DNA sequences as probes of gene expression. Cell 23:309–310.CrossRefGoogle Scholar
  33. Levis, R., Bingham, P.M., and Rubin, G.M. (1982). Physical map of the white locus of D. melanogaster. Proc. Natl. Acad. Sci. USA 79:564–568.CrossRefGoogle Scholar
  34. Lindsley, D.E. (1979). “Some developmental effects of three mutations which map within a tighly linked cluster of maternal-effect genes.” M.S. Thesis, University of Washington.Google Scholar
  35. Lis, J.T., Prestidge, L., and Hogness, D.S. (1979). A novel arrangement of tandemly repeated genes at a major heat shock site in D. melanogaster. Cell 14:910–920.Google Scholar
  36. Lohs-Schardin, M. (1982). Dicephalic—A Drosophila mutant affecting polarity in follicle cell organization and embryonic patterning. Wilhelm Roux’ Archiv. 191:28–36.CrossRefGoogle Scholar
  37. Lohs-Schardin, M., Sander, K., Cremer, C., Cremer, T., and Zorn, C. (1979a). Localized ultraviolet laser microbeam irradiation of early Drosophila embryos: fate maps based on location and frequency of adult defects. Devel. Biol. 68:533–545.CrossRefGoogle Scholar
  38. Lohs-Schardin, M. Cremer, C., and Nusslein-Volhard, C. (1979b). A fate map for the larval epidermis of Drosophila melanogaster: Localized cuticle defects following irradiation of the blastoderm with an ultraviolet laser microbeam. Devel. Biol. 73:239–255.CrossRefGoogle Scholar
  39. Lovett, J.A. and Goldstein, E.S. (1977). The cytoplasmic distribution and characterization of poly(A)+ RNA in oocytes and embryos of Drosophila. Devel. Biol. 61:70–78.CrossRefGoogle Scholar
  40. Madhavan, M.M. and Schneiderman, H.A. (1977). Histological analysis of the dynamics of growth of imaginai discs and histoblast nests during the larval development of Drosophila melanogaster. Wilhelm Roux’ Archiv. 183:269–305.CrossRefGoogle Scholar
  41. Mahowald, A.P. (1971). Polar granules of Drosophila. III. The continuity of polar granules during the life cycle of Drosophila. J. Exp. Zool. 176:329–343.CrossRefGoogle Scholar
  42. Mange, A.P. and Sandler, L. (1973). A note on the maternal effect mutants daughterless and abnormal oocyte in Drosophila melanogaster. Genetics 73:73–86.Google Scholar
  43. Rice, T.B. and Garen, A. (1975). Localized defects of blastoderm formation in maternal effect mutants of Drosophila. Devel. Biol. 43:277–286.CrossRefGoogle Scholar
  44. Roychoudhury, R., Jay, E., and Wu, R. (1976). Terminal labeling and addition of homopolymer tracts to duplex DNA fragments by terminal deoxynucleotidyl transferase. Nuc. Acids Res. 3:863–877.Google Scholar
  45. Sakoyama, Y. and Okubo, S. (1981). Two-dimensional gel patterns of protein species during development of Drosophila embryos. Devel. Biol. 81:361–365.CrossRefGoogle Scholar
  46. Sandler, L. (1972). On the genetic control of genes located in the sex-chromosome heterochromatin of Drosophila melanogaster. Genetics 70:261–274.Google Scholar
  47. Sandler, L. (1977). Evidence for a set of closely linked autosomal genes that interact with sex-chromosome heterochromatin in Drosophila melanogaster. Genetics 86:567–582.Google Scholar
  48. Santon, J.B. and Pellegrini, M. (1981). Rates of ribosomal protein and total protein synthesis during Drosophila early embryogenesis. Devel. Biol. 85:252–257.CrossRefGoogle Scholar
  49. Savoini, A. Micali, F., Marzari, R., de Cristini, F., and Grazioski, G. (1981). Low variablity of the protein species synthesized by Drosophila melanogaster embryos. Wilhelm Roux’ Archiv. 190:161–167.CrossRefGoogle Scholar
  50. Scherer, G., Telford, J., Baldani, C., and Pirrotta, V. (1981). Isolation of cloned genes differentially expressed at early and late stages of Drosophila embryonic development. Devel. Biol. 86:438–447.CrossRefGoogle Scholar
  51. Simcox, A.A. and Sang, J.H. (1983). When does determination occur in Drosophila embryos? Devel. Biol., in press.Google Scholar
  52. Sina, B.J. and Pellegrini, M. (1982). Genomic clones coding for some initial genes expressed during Drosophila development. Proc. Natl. Acad. Sci. USA 79:7351–7355.CrossRefGoogle Scholar
  53. Sonnenblick, B.P. (1950). The early embryology of Drosophila melanogaster. In “Biology of Drosophila,” M. Denerec (ed.). Hafner Publishing Co., New York.Google Scholar
  54. Struhl, G. and Brower, D. (1982). Early role of the esc + gene product in the determination of segments in Drosophila. Cell 31:285–292.CrossRefGoogle Scholar
  55. Mangiarotti, G., Chung, S., Zuker, C., and Lodish, H. (1981). Selection and analysis of cloned developmentally regulated Dictyostelium discoideum genes by hybridization competition. Nuc. Acids Res. 9:947–963.CrossRefGoogle Scholar
  56. Maxam, A.M. and Gilbert, W. (1980). Sequencing end-labeled DNA with base-specific chemical cleavages. Meth. Enzymol. 65:499–559.CrossRefGoogle Scholar
  57. McKnight, S.L. and Miller, Jr., O.L. (1976). Ultrastructural patterns of RNA synthesis during early embryogenesis of Drosophila melanogaster. Cell 8: 305–319.CrossRefGoogle Scholar
  58. Nusslein-Volhard, C. (1979). Maternal effect mutations that alter the spatial coordinates of the embryo. In “Determinants of Spatial Organization,” S. Subtelney (ed.), pp. 185–211. Academic Press, New York.Google Scholar
  59. Nusslein-Volhard, C. and Wieschaus, E. (1980). Mutations affecting segment number and polarity in Drosophila. Nature 287:795–801.CrossRefGoogle Scholar
  60. Nusslein-Volhard, C., Wieschaus, E., and Kluding, H. (1983). Lethal mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Wilhelm Roux’ Archiv., in press.Google Scholar
  61. Okada, M., Kleinman, I.A., and Schneiderman, H.A. (1974). Restoration of fertility in sterilized Drosophila eggs by transplantation of polar cytoplasm. Devel. Biol. 37:43–54.CrossRefGoogle Scholar
  62. Padayatty, J., Cummings, I., Manske, C.L., Higuchi, R., Woo, S., and Salser, W. (1981). Cloning of chicken globin cDNA in bacterial plasmids. Gene 13:417–422.CrossRefGoogle Scholar
  63. Payvar, F. and Schimke, R.T. (1979). Methylmercury hydroxide enhancement of translation and transcription of ovalbumin and conalbumin mRNAs. J. Biol. Chem. 254:7636–7642.Google Scholar
  64. Poulsen, D.F. (1950). Histogenesis, organogenesis and differentiation in the embryo of Drosophila melanogaster Meigen. In “Biology of Drosophila,” M. Demerec (ed.). Hafner Publishing Co., New York.Google Scholar
  65. Proudfoot, N.J. and Brownlee, G.G. (1976). 3’ non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214.CrossRefGoogle Scholar
  66. Queen, C. and Korn, L. (1980). Computer analysis of nucleic acids and proteins. Meth. Enzymol. 65:595–609.CrossRefGoogle Scholar
  67. Rabinowitz, M. (1941). Studies on the cytology and early embryology of the egg of Drosophila melanogaster. J. Morphol. 69:1–49.CrossRefGoogle Scholar
  68. Swanson, M.M. and Poodry, C.A. (1980). Pole cell formation in Drosophila melanogaster. Devel. Biol. 75:419–430.Google Scholar
  69. Thierry-Mieg, D. (1976). Study of a temperature-sensitive mutant grandchildless-like in Drosophila melanogaster. J. Microsc. Biol. Cell. 25:l–6.Google Scholar
  70. Thomas, P.S. (1980). Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA 77:5201–5205.CrossRefGoogle Scholar
  71. Torok, I. and Karch, F. (1980). Nucleotide sequences of heat shock activated genes in Drosophila melanogaster. I. Sequences in the regions of the 5’ and 3’ end of the hsp70 gene in the hybrid Plasmid 56H8. Nucl. Acids. Res. 8:3105–3123.CrossRefGoogle Scholar
  72. Underwood, E.M., Turner, F.R., and Mahowald, A.P. (1980). Analysis of cell movements and fate mapping during early embryogenesis in Drosophila melanogaster. Devel. Biol. 74:286–301.CrossRefGoogle Scholar
  73. Warn, R.M. and Magrath, R. (1982). Observations by a novel method of surface changes during the syncytial blastoderm stages of the Drosophila embryos. Devel. Biol. 89:540–548.CrossRefGoogle Scholar
  74. Wickens, M.P., Buell, G.N., and Schimke, R.T. (1978). Synthesis of double-stranded DNA complementary to lysozyme, ovomucoid and ovalbumin mRNAs. J. Biol. Chem. 253:2483–2495.Google Scholar
  75. Wieschaus, E. and Gehring, W. (1976). Clonal analysis of primordial disk cells in the early embryo of Drosophila melanogaster. Devel. Biol. 50:249–263.CrossRefGoogle Scholar
  76. Wright, T.R.F. (1970). The genetics of embryogenesis of Drosophila. Advan. Genet. 15:261–395.CrossRefGoogle Scholar
  77. Yen, P., Hershey, N.D., Robinson, R., and Davidson, N. (1979). Sequence organization of Drosophila tRNA genes. In “INC-UCLA Symposium on Eucaryotic Gene Regulation,” R. Axel and T. Maniatis (eds.). Academic Press, New York.Google Scholar
  78. Zalokar, M. (1976). Autoradiographic study of protein and RNA formation during early development of Drosophila eggs. Devel. Biol. 49:425–437.CrossRefGoogle Scholar
  79. Zalokar, M. Audit, C., and Erk, I. (1975). Developmental defects of female-sterile mutants of Drosophila melanogaster. Devel. Biol. 47:419–432.CrossRefGoogle Scholar
  80. Zalokar, M. and Erk, I. (1976). Division and migration of nuclei during early embryogenesis of Drosophila melanogaster. J. Microsc. Biol. Cell. 25:97–106.Google Scholar

Copyright information

© Plenum Press, New York 1984

Authors and Affiliations

  • Judith A. Lengyel
    • 1
  • Steven R. Thomas
    • 1
  • Paul David Boyer
    • 1
  • Fidel Salas
    • 1
  • Teresa R. Strecker
    • 1
  • Inyong Lee
    • 1
  • Melissa L. Graham
    • 1
  • Margaret Roark
    • 1
  • Eileen M. Underwood
    • 1
  1. 1.Molecular Biology Institute and Department of BiologyUniversity of California, Los AngeleLos AngelesUSA

Personalised recommendations