Dorsal-Ventral Gene Expression in the Drosophila Embryo Reflects the Dynamics and Precision of the Dorsal Nuclear Gradient

• Published in: Developmental cell 2012-03, Vol.22 (3), p.544-557
• Main Authors: Reeves, Gregory T., Trisnadi, Nathanie, Truong, Thai V., Nahmad, Marcos, Katz, Sophie, Stathopoulos, Angelike
• Format: Article
• Language: English
• Subjects: Animals; Biological and medical sciences; Body Patterning - genetics; Cell differentiation, maturation, development, hematopoiesis; Cell physiology; Computer applications; Computer Simulation; Development; Drosophila; Drosophila melanogaster - cytology; Drosophila melanogaster - embryology; Drosophila melanogaster - genetics; Drosophila Proteins - genetics; Embryo, Nonmammalian - metabolism; Embryogenesis; Embryos; Female; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Regulation, Developmental; Genetic diversity; Microscopy; Microscopy - methods; Molecular and cellular biology; Oscillations; Pattern formation; Plastics; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2011.12.007

Patterning of the dorsal-ventral axis in the early Drosophila embryo depends on the nuclear distribution of the Dorsal transcription factor. Using live two-photon light-sheet microscopy, we quantified the nuclear Dorsal gradient in space and time and found that its amplitude and basal levels display oscillations throughout early embryonic development. These dynamics raise questions regarding how cells can reproducibly establish patterns of gene expression from a rapidly varying signal. We therefore quantified domains of Dorsal target genes, discovering their expression patterns are also dynamic. Computational modeling of this system reveals a correlation between Dorsal gradient dynamics and changes in target gene expression and suggests that these dynamics, together with time averaging of noise, results in the formation of graded gene expression borders in regions where the gradient is nearly flat. We propose that mRNA levels remain plastic during transient signaling events, allowing tissues to refine patterns in the face of genetic or environmental variation. [Display omitted] ► The Dorsal gradient has dynamic amplitude and basal levels but constant shape ► As a result, Dorsal target genes are also dynamic, between and within nuclear cycles ► These dynamics, plus time averaging of noise, produce nonsharp domain borders ► Plasticity of mRNA expression supports refinement during pattern formation Rapid nuclear divisions early in Drosophila development prevent the Rel-family transcriptional morphogen, Dorsal, from achieving steady-state nuclear concentrations. Reeves et al. find that Dorsal target gene expression also fails to reach equilibrium. Their work suggests how pre-steady-state readouts from shallow morphogen gradients are interpreted to allow robust developmental patterning.