An essential role for zygotic expression in the pre-cellular Drosophila embryo

PLoS Genet. 2013 Apr;9(4):e1003428. doi: 10.1371/journal.pgen.1003428. Epub 2013 Apr 4.

Abstract

The Drosophila embryo proceeds through thirteen mitotic divisions as a syncytium. Its nuclei distribute in the embryo's interior during the first six divisions, dividing synchronously with a cycle time of less than ten minutes. After seven divisions (nuclear cycle 8), the syncytial blastoderm forms as the nuclei approach the embryo surface and slow their cycle time; subsequent divisions proceed in waves that initiate at the poles. Because genetic studies have not identified zygotic mutants that affect the early divisions and because transcription has not been detected before cycle 8, the early, pre-blastoderm embryo has been considered to rely entirely on maternal contributions and to be transcriptionally silent. Our studies identified several abnormal phenotypes in live engrailed (en) mutant embryos prior to cycle 8, as well as a small group of genes that are transcribed in embryos prior to cycle 7. Nuclei in en embryos divide asynchronously, an abnormality that was detected as early as nuclear cycle 2-3. Anti-En antibody detected nuclear En protein in embryos at cycle 2, and expression of an En:GFP fusion protein encoded in the paternal genome was also detected in cycle 2 nuclei. These findings demonstrate that the Drosophila embryo is functionally competent for gene expression prior to the onset of its rapid nuclear divisions and that the embryo requires functions that are expressed in the zygote in order to faithfully prosecute its early, pre-cellularization mitotic cycles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blastoderm / cytology
  • Cell Division / genetics*
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Drosophila Proteins
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / genetics
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Morphogenesis / genetics*
  • Mutation
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism
  • Zygote / cytology
  • Zygote / metabolism

Substances

  • Drosophila Proteins
  • En protein, Drosophila
  • Homeodomain Proteins
  • Transcription Factors