Abstract
The morphogenesis of structures with repeated functional units, such as body segments and appendages, depends on multi-domain patterns of cell signaling and gene expression. We demonstrate that during Drosophila oogenesis, the two-domain expression pattern of Broad, a transcription factor essential for the formation of the two respiratory eggshell appendages, is established by a single gradient of EGFR activation that induces both Broad and Pointed, which mediates repression of Broad. Two negative-feedback loops provided by the intracellular inhibitors of EGFR signaling, Kekkon-1 and Sprouty, control the number and position of Broad-expressing cells and in this way influence eggshell morphology. Later in oogenesis, the gradient of EGFR activation is split into two smaller domains in a process that depends on Argos, a secreted antagonist of EGFR signaling. In contrast to the previously proposed model of eggshell patterning, we show that the two-domain pattern of EGFR signaling is not essential for specifying the number of appendages. Thus, the processes that define the two-domain patterns of Broad and EGFR activation are distinct; their actions are separated in time and have different effects on eggshell morphology.
Publication types
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Research Support, N.I.H., Extramural
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Research Support, Non-U.S. Gov't
MeSH terms
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Animals
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Body Patterning / physiology*
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DNA-Binding Proteins / genetics
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DNA-Binding Proteins / metabolism
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Drosophila Proteins / genetics
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Drosophila Proteins / metabolism*
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Drosophila melanogaster / anatomy & histology
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Drosophila melanogaster / embryology*
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Drosophila melanogaster / physiology
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Enzyme Activation
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ErbB Receptors / genetics
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ErbB Receptors / metabolism*
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Eye Proteins / genetics
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Eye Proteins / metabolism
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Feedback, Physiological / physiology*
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Female
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MAP Kinase Signaling System / physiology*
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Membrane Proteins / genetics
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Membrane Proteins / metabolism
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Mitogen-Activated Protein Kinases / metabolism
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Nerve Tissue Proteins / genetics
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Nerve Tissue Proteins / metabolism
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Oogenesis / physiology*
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Protein Tyrosine Phosphatases / genetics
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Protein Tyrosine Phosphatases / metabolism
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Proto-Oncogene Proteins / genetics
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Proto-Oncogene Proteins / metabolism
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Transcription Factors / genetics
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Transcription Factors / metabolism*
Substances
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Br protein, Drosophila
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DNA-Binding Proteins
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Drosophila Proteins
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Eye Proteins
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Membrane Proteins
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Nerve Tissue Proteins
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Proto-Oncogene Proteins
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Transcription Factors
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pnt protein, Drosophila
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sty protein, Drosophila
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aos protein, Drosophila
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ErbB Receptors
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Mitogen-Activated Protein Kinases
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Kek1 protein, Drosophila
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Protein Tyrosine Phosphatases