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Orthodenticle Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Drosophila Retina.

Mencarelli C, Pichaud F - PLoS Genet. (2015)

Bottom Line: Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo).In addition, we find that otd regulates synaptic-layer targeting of R8.Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

View Article: PubMed Central - PubMed

Affiliation: MRC Laboratory for Molecular Cell Biology, University College London, London, United Kingdom.

ABSTRACT
Parallel processing of neuronal inputs relies on assembling neural circuits into distinct synaptic-columns and layers. This is orchestrated by matching recognition molecules between afferent growth cones and target areas. Controlling the expression of these molecules during development is crucial but not well understood. The developing Drosophila visual system is a powerful genetic model for addressing this question. In this model system, the achromatic R1-6 photoreceptors project their axons in the lamina while the R7 and R8 photoreceptors, which are involved in colour detection, project their axons to two distinct synaptic-layers in the medulla. Here we show that the conserved homeodomain transcription factor Orthodenticle (Otd), which in the eye is a main regulator of rhodopsin expression, is also required for R1-6 photoreceptor synaptic-column specific innervation of the lamina. Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo). In addition, we find that otd regulates synaptic-layer targeting of R8. We demonstrate that during this process, otd and the R8-specific transcription factor senseless/Gfi1 (sens) function as independent transcriptional inputs that are required for the expression of fmi, gogo and the adhesion molecule capricious (caps), which govern R8 synaptic-layer targeting. Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

No MeSH data available.


Related in: MedlinePlus

Schematic representation of the Drosophila visual system.(A) Schematic representation of Drosophila axonal photoreceptor projections in the third instar larva optic lobe. The outer R1-R6 (indicated in light blue) from each ommatidium in the eye disc project their axons into the lamina part of the brain. At this early developmental stage, the inner photoreceptor R8s (yellow) project through the lamina and establish a regular retinotopic array of terminals in the medulla. (B) Schematic representation of the adult Drosophila visual system. R-cell axons are organized into synaptic-columns and layers. Six different photoreceptors (indicated in light blue) from six neighbouring ommatidia share the same optical axis and pool their axons in the same synaptic-column in the lamina [2]. R8 (orange) and R7 (green) photoreceptor axons pass through the lamina and terminate in distinct synaptic-layers M3 (R8) and M6 (R7).
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pgen.1005303.g001: Schematic representation of the Drosophila visual system.(A) Schematic representation of Drosophila axonal photoreceptor projections in the third instar larva optic lobe. The outer R1-R6 (indicated in light blue) from each ommatidium in the eye disc project their axons into the lamina part of the brain. At this early developmental stage, the inner photoreceptor R8s (yellow) project through the lamina and establish a regular retinotopic array of terminals in the medulla. (B) Schematic representation of the adult Drosophila visual system. R-cell axons are organized into synaptic-columns and layers. Six different photoreceptors (indicated in light blue) from six neighbouring ommatidia share the same optical axis and pool their axons in the same synaptic-column in the lamina [2]. R8 (orange) and R7 (green) photoreceptor axons pass through the lamina and terminate in distinct synaptic-layers M3 (R8) and M6 (R7).

Mentions: The Drosophila compound eye has long served as a powerful system to dissect the genetic and molecular basis for establishing neural circuits during development. Each of the 750 facet lenses (i.e., ommatidia) that form the fly eye contains six outer photoreceptors (R1-R6) and two inner photoreceptors (R7 and R8). R1-R6 are involved in motion detection and express the broad-spectrum Rhodopsin1 (Rh1) [1]. These photoreceptors project axons and form synapses in the lamina, a ganglion that lies directly below the retina. Neural wiring of the outer photoreceptors in the lamina follows the principle of neural superposition, where six neighbouring ommatidia each project one outer photoreceptor terminal to one given synaptic-column (Fig 1) [2,3]. R7 and R8 are involved in chromatic discrimination and express different rhodopsin genes. R7 photoreceptors express either the UV-rhodopsin rh3 or rh4 [4], whereas R8 photoreceptors express either the blue rh5 or green-rh6 [5,6]. Within each ommatidium, the light-gathering organelle of R7 shares its optical axis with that of the underlying R8 photoreceptor. Therefore, these two neurons can compare the chromatic composition of the incident light. In this context, each pair of R7/R8 axons is found within one column but their respective growth cones establish synaptic connections in distinct synaptic-layers (Fig 1B). R8 axons terminate within the superficial M3 layer and R7 axons terminate deeper in the medulla, in the M6 layer.


Orthodenticle Is Required for the Expression of Principal Recognition Molecules That Control Axon Targeting in the Drosophila Retina.

Mencarelli C, Pichaud F - PLoS Genet. (2015)

Schematic representation of the Drosophila visual system.(A) Schematic representation of Drosophila axonal photoreceptor projections in the third instar larva optic lobe. The outer R1-R6 (indicated in light blue) from each ommatidium in the eye disc project their axons into the lamina part of the brain. At this early developmental stage, the inner photoreceptor R8s (yellow) project through the lamina and establish a regular retinotopic array of terminals in the medulla. (B) Schematic representation of the adult Drosophila visual system. R-cell axons are organized into synaptic-columns and layers. Six different photoreceptors (indicated in light blue) from six neighbouring ommatidia share the same optical axis and pool their axons in the same synaptic-column in the lamina [2]. R8 (orange) and R7 (green) photoreceptor axons pass through the lamina and terminate in distinct synaptic-layers M3 (R8) and M6 (R7).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482733&req=5

pgen.1005303.g001: Schematic representation of the Drosophila visual system.(A) Schematic representation of Drosophila axonal photoreceptor projections in the third instar larva optic lobe. The outer R1-R6 (indicated in light blue) from each ommatidium in the eye disc project their axons into the lamina part of the brain. At this early developmental stage, the inner photoreceptor R8s (yellow) project through the lamina and establish a regular retinotopic array of terminals in the medulla. (B) Schematic representation of the adult Drosophila visual system. R-cell axons are organized into synaptic-columns and layers. Six different photoreceptors (indicated in light blue) from six neighbouring ommatidia share the same optical axis and pool their axons in the same synaptic-column in the lamina [2]. R8 (orange) and R7 (green) photoreceptor axons pass through the lamina and terminate in distinct synaptic-layers M3 (R8) and M6 (R7).
Mentions: The Drosophila compound eye has long served as a powerful system to dissect the genetic and molecular basis for establishing neural circuits during development. Each of the 750 facet lenses (i.e., ommatidia) that form the fly eye contains six outer photoreceptors (R1-R6) and two inner photoreceptors (R7 and R8). R1-R6 are involved in motion detection and express the broad-spectrum Rhodopsin1 (Rh1) [1]. These photoreceptors project axons and form synapses in the lamina, a ganglion that lies directly below the retina. Neural wiring of the outer photoreceptors in the lamina follows the principle of neural superposition, where six neighbouring ommatidia each project one outer photoreceptor terminal to one given synaptic-column (Fig 1) [2,3]. R7 and R8 are involved in chromatic discrimination and express different rhodopsin genes. R7 photoreceptors express either the UV-rhodopsin rh3 or rh4 [4], whereas R8 photoreceptors express either the blue rh5 or green-rh6 [5,6]. Within each ommatidium, the light-gathering organelle of R7 shares its optical axis with that of the underlying R8 photoreceptor. Therefore, these two neurons can compare the chromatic composition of the incident light. In this context, each pair of R7/R8 axons is found within one column but their respective growth cones establish synaptic connections in distinct synaptic-layers (Fig 1B). R8 axons terminate within the superficial M3 layer and R7 axons terminate deeper in the medulla, in the M6 layer.

Bottom Line: Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo).In addition, we find that otd regulates synaptic-layer targeting of R8.Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

View Article: PubMed Central - PubMed

Affiliation: MRC Laboratory for Molecular Cell Biology, University College London, London, United Kingdom.

ABSTRACT
Parallel processing of neuronal inputs relies on assembling neural circuits into distinct synaptic-columns and layers. This is orchestrated by matching recognition molecules between afferent growth cones and target areas. Controlling the expression of these molecules during development is crucial but not well understood. The developing Drosophila visual system is a powerful genetic model for addressing this question. In this model system, the achromatic R1-6 photoreceptors project their axons in the lamina while the R7 and R8 photoreceptors, which are involved in colour detection, project their axons to two distinct synaptic-layers in the medulla. Here we show that the conserved homeodomain transcription factor Orthodenticle (Otd), which in the eye is a main regulator of rhodopsin expression, is also required for R1-6 photoreceptor synaptic-column specific innervation of the lamina. Our data indicate that otd function in these photoreceptors is largely mediated by the recognition molecules flamingo (fmi) and golden goal (gogo). In addition, we find that otd regulates synaptic-layer targeting of R8. We demonstrate that during this process, otd and the R8-specific transcription factor senseless/Gfi1 (sens) function as independent transcriptional inputs that are required for the expression of fmi, gogo and the adhesion molecule capricious (caps), which govern R8 synaptic-layer targeting. Our work therefore demonstrates that otd is a main component of the gene regulatory network that regulates synaptic-column and layer targeting in the fly visual system.

No MeSH data available.


Related in: MedlinePlus