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Dpp Signaling Activity Requires Pentagone to Scale with Tissue Size in the Growing Drosophila Wing Imaginal Disc

Authors: Sven Bergmann; Sven Bergmann; George Pyrowolakis; Aitana Morton de Lachapelle; Aitana Morton de Lachapelle; Fisun Hamaratoglu; Markus Affolter;

Dpp Signaling Activity Requires Pentagone to Scale with Tissue Size in the Growing Drosophila Wing Imaginal Disc

Abstract

The wing of the fruit fly, Drosophila melanogaster, with its simple, two-dimensional structure, is a model organ well suited for a systems biology approach. The wing arises from an epithelial sac referred to as the wing imaginal disc, which undergoes a phase of massive growth and concomitant patterning during larval stages. The Decapentaplegic (Dpp) morphogen plays a central role in wing formation with its ability to co-coordinately regulate patterning and growth. Here, we asked whether the Dpp signaling activity scales, i.e. expands proportionally, with the growing wing imaginal disc. Using new methods for spatial and temporal quantification of Dpp activity and its scaling properties, we found that the Dpp response scales with the size of the growing tissue. Notably, scaling is not perfect at all positions in the field and the scaling of target gene domains is ensured specifically where they define vein positions. We also found that the target gene domains are not defined at constant concentration thresholds of the downstream Dpp activity gradients P-Mad and Brinker. Most interestingly, Pentagone, an important secreted feedback regulator of the pathway, plays a central role in scaling and acts as an expander of the Dpp gradient during disc growth.

Countries
Germany, Switzerland
Keywords

Male, SX20 Research, Technology and Development Projects, QH301-705.5, Recombinant Fusion Proteins, Green Fluorescent Proteins, Nerve Tissue Proteins, 1100 General Agricultural and Biological Sciences, SX00 SystemsX.ch, SX15 WingX, 1300 General Biochemistry, Genetics and Molecular Biology, 2400 General Immunology and Microbiology, Morphogenesis, Animals, Drosophila Proteins, Wings, Animal, Biology (General), Phosphorylation, Homeodomain Proteins, Extracellular Matrix Proteins, 2800 General Neuroscience, Animals; DNA-Binding Proteins/metabolism; Drosophila Proteins/metabolism; Drosophila melanogaster/growth & development; Drosophila melanogaster/metabolism; Extracellular Matrix Proteins/metabolism; Female; Green Fluorescent Proteins/metabolism; Homeodomain Proteins/metabolism; Larva/growth & development; Larva/metabolism; Male; Microscopy, Fluorescence; Morphogenesis; Nerve Tissue Proteins/metabolism; Organ Size; Phosphorylation; Recombinant Fusion Proteins/metabolism; Repressor Proteins/metabolism; T-Box Domain Proteins/metabolism; Transcription Factors/metabolism; Wing/blood supply; Wing/growth & development, Organ Size, DNA-Binding Proteins, Repressor Proteins, Drosophila melanogaster, Microscopy, Fluorescence, Larva, 570 Life sciences; biology, Female, T-Box Domain Proteins, Research Article, Transcription Factors

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    citations
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    111
    popularity
    This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
    Top 10%
    influence
    This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
    Top 10%
    impulse
    This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
    Top 10%
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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
111
Top 10%
Top 10%
Top 10%
Green
gold