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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

Caps expression is downregulated in otduvi mutant R8 photoreceptors.Side view of wild-type (A) and otduvi mutant (B) third instar larva eye disc revealing that caps expression is strongly reduced in otd mutant R8. The expression of mCD8-GFP is under the control of caps-Gal4 [8]. Elav (blue) and 24B10 (red) stain the full set of photoreceptors. (C) Representation of an ommatidium showing the basal localization of the R8 photoreceptor in green. Expression of Caps (green) in wild-type (D, D’) and otduvi mutant (E, E’) optic lobes (60% after puparium formation). Photoreceptor-cell-axons are stained with the 24B10 antibody. The R8 (M3) and R7 (M6) recipient layers are indicated by dashed lines in this and the following figures. When compared to wild-type, otduvi mutant retina show a reproducible gap pattern detected in the R8 layer (M3) (D’, E’). These gaps correspond to a loss of Caps expression in the afferent R8 axons (boxed in E and magnified in E’).
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pgen.1005303.g004: Caps expression is downregulated in otduvi mutant R8 photoreceptors.Side view of wild-type (A) and otduvi mutant (B) third instar larva eye disc revealing that caps expression is strongly reduced in otd mutant R8. The expression of mCD8-GFP is under the control of caps-Gal4 [8]. Elav (blue) and 24B10 (red) stain the full set of photoreceptors. (C) Representation of an ommatidium showing the basal localization of the R8 photoreceptor in green. Expression of Caps (green) in wild-type (D, D’) and otduvi mutant (E, E’) optic lobes (60% after puparium formation). Photoreceptor-cell-axons are stained with the 24B10 antibody. The R8 (M3) and R7 (M6) recipient layers are indicated by dashed lines in this and the following figures. When compared to wild-type, otduvi mutant retina show a reproducible gap pattern detected in the R8 layer (M3) (D’, E’). These gaps correspond to a loss of Caps expression in the afferent R8 axons (boxed in E and magnified in E’).

Mentions: Processing of chromatic information relies on R7 and R8 establishing their synapses in two distinct layers of the medulla (Fig 1B and S1 Fig). In R8, layer-specific targeting relies on the expression of fmi, gogo and caps, amongst other adhesion and recognition molecules. Interestingly, similar to fmi and gogo, we find that the mRNA levels for caps are greatly reduced in otd mutant retina (Fig 3H). This reduction is also observed in R8 using an in vivo reporter gene for the caps locus, capsGal4-UASGFP [8] (Fig 4A and 4B). In addition, the Caps protein is no longer detected in the otd mutant R8 axons, leading to gaps in expression at the M3 layer, where the R8 axons normally terminate (Fig 4D and 4E’). Therefore, otd is required for the expression of key recognition molecules and CAMs that are known to govern the layer-specific targeting of R8.


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)

Caps expression is downregulated in otduvi mutant R8 photoreceptors.Side view of wild-type (A) and otduvi mutant (B) third instar larva eye disc revealing that caps expression is strongly reduced in otd mutant R8. The expression of mCD8-GFP is under the control of caps-Gal4 [8]. Elav (blue) and 24B10 (red) stain the full set of photoreceptors. (C) Representation of an ommatidium showing the basal localization of the R8 photoreceptor in green. Expression of Caps (green) in wild-type (D, D’) and otduvi mutant (E, E’) optic lobes (60% after puparium formation). Photoreceptor-cell-axons are stained with the 24B10 antibody. The R8 (M3) and R7 (M6) recipient layers are indicated by dashed lines in this and the following figures. When compared to wild-type, otduvi mutant retina show a reproducible gap pattern detected in the R8 layer (M3) (D’, E’). These gaps correspond to a loss of Caps expression in the afferent R8 axons (boxed in E and magnified in E’).
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pgen.1005303.g004: Caps expression is downregulated in otduvi mutant R8 photoreceptors.Side view of wild-type (A) and otduvi mutant (B) third instar larva eye disc revealing that caps expression is strongly reduced in otd mutant R8. The expression of mCD8-GFP is under the control of caps-Gal4 [8]. Elav (blue) and 24B10 (red) stain the full set of photoreceptors. (C) Representation of an ommatidium showing the basal localization of the R8 photoreceptor in green. Expression of Caps (green) in wild-type (D, D’) and otduvi mutant (E, E’) optic lobes (60% after puparium formation). Photoreceptor-cell-axons are stained with the 24B10 antibody. The R8 (M3) and R7 (M6) recipient layers are indicated by dashed lines in this and the following figures. When compared to wild-type, otduvi mutant retina show a reproducible gap pattern detected in the R8 layer (M3) (D’, E’). These gaps correspond to a loss of Caps expression in the afferent R8 axons (boxed in E and magnified in E’).
Mentions: Processing of chromatic information relies on R7 and R8 establishing their synapses in two distinct layers of the medulla (Fig 1B and S1 Fig). In R8, layer-specific targeting relies on the expression of fmi, gogo and caps, amongst other adhesion and recognition molecules. Interestingly, similar to fmi and gogo, we find that the mRNA levels for caps are greatly reduced in otd mutant retina (Fig 3H). This reduction is also observed in R8 using an in vivo reporter gene for the caps locus, capsGal4-UASGFP [8] (Fig 4A and 4B). In addition, the Caps protein is no longer detected in the otd mutant R8 axons, leading to gaps in expression at the M3 layer, where the R8 axons normally terminate (Fig 4D and 4E’). Therefore, otd is required for the expression of key recognition molecules and CAMs that are known to govern the layer-specific targeting of R8.

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