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Chromatin Modulatory Proteins and Olfactory Receptor Signaling in the Refinement and Maintenance of Fruitless Expression in Olfactory Receptor Neurons.

Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC - PLoS Biol. (2016)

Bottom Line: This regulation requires the chromatin modulatory protein Alhambra (Alh).Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs.Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
During development, sensory neurons must choose identities that allow them to detect specific signals and connect with appropriate target neurons. Ultimately, these sensory neurons will successfully integrate into appropriate neural circuits to generate defined motor outputs, or behavior. This integration requires a developmental coordination between the identity of the neuron and the identity of the circuit. The mechanisms that underlie this coordination are currently unknown. Here, we describe two modes of regulation that coordinate the sensory identities of Drosophila melanogaster olfactory receptor neurons (ORNs) involved in sex-specific behaviors with the sex-specific behavioral circuit identity marker fruitless (fru). The first mode involves a developmental program that coordinately restricts to appropriate ORNs the expression of fru and two olfactory receptors (Or47b and Ir84a) involved in sex-specific behaviors. This regulation requires the chromatin modulatory protein Alhambra (Alh). The second mode relies on the signaling from the olfactory receptors through CamK and histone acetyl transferase p300/CBP to maintain ORN-specific fru expression. Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs. Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

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Onset of fru in developing ORNs overlaps with Or47b but is independent of Or47b function.(A) Wild-type antennae expressing fruGal4 UAS-Redstinger (magenta) and Or47b-CD8GFP (green). (B) Wild-type antennae expressing fruGal4 40XUASCD8GFP. (C)Or47b mutant antennae expressing fruGal4 40XUASCD8GFP. (D)orco mutant antennae expressing fruGal4 40XUASCD8GFP.GENOTYPES:(A) Or47b-CD8GFP/+; fruGAL4 UAS-RedStinger/+(B) +/+; fruGAL4 UAS-40XCD8GFP(C) Or47b2/Or47b2; fruGAL4 UAS-40XCD8GFP(D) orco2/orco2; fruGAL4 UAS-40XCD8GFP
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pbio.1002443.g007: Onset of fru in developing ORNs overlaps with Or47b but is independent of Or47b function.(A) Wild-type antennae expressing fruGal4 UAS-Redstinger (magenta) and Or47b-CD8GFP (green). (B) Wild-type antennae expressing fruGal4 40XUASCD8GFP. (C)Or47b mutant antennae expressing fruGal4 40XUASCD8GFP. (D)orco mutant antennae expressing fruGal4 40XUASCD8GFP.GENOTYPES:(A) Or47b-CD8GFP/+; fruGAL4 UAS-RedStinger/+(B) +/+; fruGAL4 UAS-40XCD8GFP(C) Or47b2/Or47b2; fruGAL4 UAS-40XCD8GFP(D) orco2/orco2; fruGAL4 UAS-40XCD8GFP

Mentions: We predicted that both fru and Or expression must be established in pupal stages as ORNs adopt their final fates (Fig 4A). In wild type flies, the onset of fru expression coincides with the onset of Or47b expression, starting around 40 h APF and absent at earlier stages (Fig 7A). Given the temporal coordination of Or47b expression with fru during pupal development, we wanted to test whether Or47b function is required for the onset of fru expression. To do this, we analyzed fru expression during pupal development in Or47b and orco mutants (Fig 7). In these mutants, we found that fru expression in Or47b ORNs was still detectable by 90 h APF, suggesting that OR function is not required to initiate fru expression and that other factors, such as Alh, establish the correct expression and coupling of fru/Or during ORN development (Fig 7C and 7D). However, fru expression was lost within a few days after eclosion in both Or47b and orco mutants (Fig 7C and 7D). These results indicate that Or47b function is dispensable during the onset of fru expression in pupal stages, but once the flies eclose from their pupal cases, Or47b activity is required to maintain fru expression.


Chromatin Modulatory Proteins and Olfactory Receptor Signaling in the Refinement and Maintenance of Fruitless Expression in Olfactory Receptor Neurons.

Hueston CE, Olsen D, Li Q, Okuwa S, Peng B, Wu J, Volkan PC - PLoS Biol. (2016)

Onset of fru in developing ORNs overlaps with Or47b but is independent of Or47b function.(A) Wild-type antennae expressing fruGal4 UAS-Redstinger (magenta) and Or47b-CD8GFP (green). (B) Wild-type antennae expressing fruGal4 40XUASCD8GFP. (C)Or47b mutant antennae expressing fruGal4 40XUASCD8GFP. (D)orco mutant antennae expressing fruGal4 40XUASCD8GFP.GENOTYPES:(A) Or47b-CD8GFP/+; fruGAL4 UAS-RedStinger/+(B) +/+; fruGAL4 UAS-40XCD8GFP(C) Or47b2/Or47b2; fruGAL4 UAS-40XCD8GFP(D) orco2/orco2; fruGAL4 UAS-40XCD8GFP
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4836687&req=5

pbio.1002443.g007: Onset of fru in developing ORNs overlaps with Or47b but is independent of Or47b function.(A) Wild-type antennae expressing fruGal4 UAS-Redstinger (magenta) and Or47b-CD8GFP (green). (B) Wild-type antennae expressing fruGal4 40XUASCD8GFP. (C)Or47b mutant antennae expressing fruGal4 40XUASCD8GFP. (D)orco mutant antennae expressing fruGal4 40XUASCD8GFP.GENOTYPES:(A) Or47b-CD8GFP/+; fruGAL4 UAS-RedStinger/+(B) +/+; fruGAL4 UAS-40XCD8GFP(C) Or47b2/Or47b2; fruGAL4 UAS-40XCD8GFP(D) orco2/orco2; fruGAL4 UAS-40XCD8GFP
Mentions: We predicted that both fru and Or expression must be established in pupal stages as ORNs adopt their final fates (Fig 4A). In wild type flies, the onset of fru expression coincides with the onset of Or47b expression, starting around 40 h APF and absent at earlier stages (Fig 7A). Given the temporal coordination of Or47b expression with fru during pupal development, we wanted to test whether Or47b function is required for the onset of fru expression. To do this, we analyzed fru expression during pupal development in Or47b and orco mutants (Fig 7). In these mutants, we found that fru expression in Or47b ORNs was still detectable by 90 h APF, suggesting that OR function is not required to initiate fru expression and that other factors, such as Alh, establish the correct expression and coupling of fru/Or during ORN development (Fig 7C and 7D). However, fru expression was lost within a few days after eclosion in both Or47b and orco mutants (Fig 7C and 7D). These results indicate that Or47b function is dispensable during the onset of fru expression in pupal stages, but once the flies eclose from their pupal cases, Or47b activity is required to maintain fru expression.

Bottom Line: This regulation requires the chromatin modulatory protein Alhambra (Alh).Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs.Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
During development, sensory neurons must choose identities that allow them to detect specific signals and connect with appropriate target neurons. Ultimately, these sensory neurons will successfully integrate into appropriate neural circuits to generate defined motor outputs, or behavior. This integration requires a developmental coordination between the identity of the neuron and the identity of the circuit. The mechanisms that underlie this coordination are currently unknown. Here, we describe two modes of regulation that coordinate the sensory identities of Drosophila melanogaster olfactory receptor neurons (ORNs) involved in sex-specific behaviors with the sex-specific behavioral circuit identity marker fruitless (fru). The first mode involves a developmental program that coordinately restricts to appropriate ORNs the expression of fru and two olfactory receptors (Or47b and Ir84a) involved in sex-specific behaviors. This regulation requires the chromatin modulatory protein Alhambra (Alh). The second mode relies on the signaling from the olfactory receptors through CamK and histone acetyl transferase p300/CBP to maintain ORN-specific fru expression. Our results highlight two feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs. Such a dual mechanism of fru regulation in ORNs might be a trait of neurons driving plastic aspects of sex-specific behaviors.

Show MeSH