Dorsal-Ventral Gene Expression in the Drosophila Embryo Reflects the Dynamics and Precision of the Dorsal Nuclear Gradient
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...
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Published in | Developmental cell Vol. 22; no. 3; pp. 544 - 557 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Cambridge, MA
Elsevier Inc
13.03.2012
Cell Press |
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Abstract | 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.
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► 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. |
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AbstractList | 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. 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. 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. |
Author | Stathopoulos, Angelike Reeves, Gregory T. Katz, Sophie Truong, Thai V. Trisnadi, Nathanie Nahmad, Marcos |
AuthorAffiliation | 1 Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA 2 Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA 3 Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, NC 27695, USA |
AuthorAffiliation_xml | – name: 2 Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA – name: 1 Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA – name: 3 Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, NC 27695, USA |
Author_xml | – sequence: 1 givenname: Gregory T. surname: Reeves fullname: Reeves, Gregory T. organization: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 2 givenname: Nathanie surname: Trisnadi fullname: Trisnadi, Nathanie organization: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 3 givenname: Thai V. surname: Truong fullname: Truong, Thai V. organization: Beckman Institute, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 4 givenname: Marcos surname: Nahmad fullname: Nahmad, Marcos organization: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 5 givenname: Sophie surname: Katz fullname: Katz, Sophie organization: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 6 givenname: Angelike surname: Stathopoulos fullname: Stathopoulos, Angelike email: angelike@caltech.edu organization: Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA |
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Keywords | Embryo Gradient Arthropoda Insecta Development Invertebrata Gene expression Drosophila melanogaster Diptera Drosophilidae |
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Snippet | Patterning of the dorsal-ventral axis in the early Drosophila embryo depends on the nuclear distribution of the Dorsal transcription factor. Using live... Patterning of the dorsal-ventral axis in the early Drosophila embryo depends on the nuclear distribution of the Dorsal transcription factor. Using live... |
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SubjectTerms | 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 |
Title | Dorsal-Ventral Gene Expression in the Drosophila Embryo Reflects the Dynamics and Precision of the Dorsal Nuclear Gradient |
URI | https://dx.doi.org/10.1016/j.devcel.2011.12.007 https://www.ncbi.nlm.nih.gov/pubmed/22342544 https://search.proquest.com/docview/1028020554 https://search.proquest.com/docview/928907282 https://pubmed.ncbi.nlm.nih.gov/PMC3469262 |
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