Multiscale diffusion in the mitotic Drosophila melanogaster syncytial blastoderm

Proc Natl Acad Sci U S A. 2012 May 29;109(22):8588-93. doi: 10.1073/pnas.1204270109. Epub 2012 May 16.

Abstract

Despite the fundamental importance of diffusion for embryonic morphogen gradient formation in the early Drosophila melanogaster embryo, there remains controversy regarding both the extent and the rate of diffusion of well-characterized morphogens. Furthermore, the recent observation of diffusional "compartmentalization" has suggested that diffusion may in fact be nonideal and mediated by an as-yet-unidentified mechanism. Here, we characterize the effects of the geometry of the early syncytial Drosophila embryo on the effective diffusivity of cytoplasmic proteins. Our results demonstrate that the presence of transient mitotic membrane furrows results in a multiscale diffusion effect that has a significant impact on effective diffusion rates across the embryo. Using a combination of live-cell experiments and computational modeling, we characterize these effects and relate effective bulk diffusion rates to instantaneous diffusion coefficients throughout the syncytial blastoderm nuclear cycle phase of the early embryo. This multiscale effect may be related to the effect of interphase nuclei on effective diffusion, and thus we propose that an as-yet-unidentified role of syncytial membrane furrows is to temporally regulate bulk embryonic diffusion rates to balance the multiscale effect of interphase nuclei, which ultimately stabilizes the shapes of various morphogen gradients.

MeSH terms

  • Algorithms
  • Animals
  • Animals, Genetically Modified
  • Blastoderm / cytology
  • Blastoderm / embryology
  • Blastoderm / metabolism*
  • Cell Compartmentation
  • Cell Membrane / metabolism
  • Computer Simulation
  • Cytoplasm / metabolism
  • Diffusion
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / embryology
  • Embryo, Nonmammalian / metabolism
  • Fluorescence Recovery After Photobleaching
  • Giant Cells / cytology
  • Giant Cells / metabolism*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Kinetics
  • Microscopy, Fluorescence
  • Mitosis*
  • Models, Biological

Substances

  • Green Fluorescent Proteins