Abstract
The central nervous system develops from monolayered neuroepithelial sheets. In a first step patterning mechanisms subdivide the seemingly uniform epithelia into domains allowing an increase of neuronal diversity in a tightly controlled spatial and temporal manner. In Drosophila, neuroepithelial patterning of the embryonic optic placode gives rise to the larval eye primordium, consisting of two photoreceptor (PR) precursor types (primary and secondary), as well as the optic lobe primordium, which during larval and pupal stages develops into the prominent optic ganglia. Here, we characterize a genetic network that regulates the balance between larval eye and optic lobe precursors, as well as between primary and secondary PR precursors. In a first step the proneural factor Atonal (Ato) specifies larval eye precursors, while the orphan nuclear receptor Tailless (Tll) is crucial for the specification of optic lobe precursors. The Hedgehog and Notch signaling pathways act upstream of Ato and Tll to coordinate neural precursor specification in a timely manner. The correct spatial placement of the boundary between Ato and Tll in turn is required to control the precise number of primary and secondary PR precursors. In a second step, Notch signaling also controls a binary cell fate decision, thus, acts at the top of a cascade of transcription factor interactions to define PR subtype identity. Our model serves as an example of how combinatorial action of cell extrinsic and cell intrinsic factors control neural tissue patterning.
Publication types
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Research Support, Non-U.S. Gov't
MeSH terms
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Animals
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Animals, Genetically Modified
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Basic Helix-Loop-Helix Transcription Factors / genetics
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Basic Helix-Loop-Helix Transcription Factors / metabolism
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Body Patterning / genetics
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Drosophila Proteins / genetics
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Drosophila Proteins / metabolism
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Drosophila melanogaster / genetics*
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Drosophila melanogaster / growth & development*
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Drosophila melanogaster / metabolism
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Eye / growth & development*
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Eye / metabolism*
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Gene Expression Regulation, Developmental
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Gene Regulatory Networks
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Genes, Insect
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Hedgehog Proteins / genetics
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Hedgehog Proteins / metabolism
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Larva / genetics
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Larva / growth & development
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Larva / metabolism
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Mutation
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Nerve Tissue Proteins / genetics
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Nerve Tissue Proteins / metabolism
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Neuroepithelial Cells / metabolism
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Optic Lobe, Nonmammalian / growth & development
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Optic Lobe, Nonmammalian / metabolism
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Photoreceptor Cells, Invertebrate / cytology
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Photoreceptor Cells, Invertebrate / metabolism
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Receptors, Notch / genetics
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Receptors, Notch / metabolism
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Repressor Proteins / genetics
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Repressor Proteins / metabolism
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Signal Transduction
Substances
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Basic Helix-Loop-Helix Transcription Factors
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Drosophila Proteins
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Hedgehog Proteins
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N protein, Drosophila
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Nerve Tissue Proteins
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Receptors, Notch
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Repressor Proteins
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TLL protein, Drosophila
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ato protein, Drosophila
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hh protein, Drosophila
Grants and funding
The current project is supported by the Swiss National Science foundation (
http://www.snf.ch/, project number: 31003A_169993). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.