Drosophila Auditory Organ Genes and Genetic Hearing Defects

Senthilan, Pingkalai R.; Piepenbrock, David; Ovezmyradov, Guvanch; Nadrowski, Björn; Bechstedt, Susanne; Pauls, Stephanie; Winkler, Margret; Möbius, Wiebke; Howard, Jonathon; Göpfert, Martin C.

doi:10.1016/j.cell.2012.06.043

Cited by 200 publications

(262 citation statements)

References 97 publications

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“…While our work is the first description of this opsin expression pattern in mollusks, opsin-expressing mechanoreceptors have been recently described in the annelid Platynereis, zebrafish and Drosophila (Backfisch et al, 2013;Senthilan et al, 2012). From work on mechanoreception in Drosophila antennae, we now know that opsin is required for anntenal mechanoreceptors to detect vibrations, highlighting a previously unknown role for opsin in senses besides light detection (Senthilan et al, 2012). We do not yet know whether the opsin-expressing cells we found in hatchling O. bimaculoides skin function as mechanoreceptors, light sensors or both, or the extent to which opsin is required for detecting either of these stimuli.…”

Section: Discussionmentioning

confidence: 89%

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

Ramirez

Oakley

2015

Journal of Experimental Biology

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Cephalopods are renowned for changing the color and pattern of their skin for both camouflage and communication. Yet, we do not fully understand how cephalopods control the pigmented chromatophore organs in their skin and change their body pattern. Although these changes primarily rely on eyesight, we found that light causes chromatophores to expand in excised pieces of Octopus bimaculoides skin. We call this behavior light-activated chromatophore expansion (or LACE). To uncover how octopus skin senses light, we used antibodies against r-opsin phototransduction proteins to identify sensory neurons that express r-opsin in the skin. We hypothesized that octopus LACE relies on the same r-opsin phototransduction cascade found in octopus eyes. By creating an action spectrum for the latency to LACE, we found that LACE occurred most quickly in response to blue light. We fit our action spectrum data to a standard opsin curve template and estimated the λ max of LACE to be 480 nm. Consistent with our hypothesis, the maximum sensitivity of the light sensors underlying LACE closely matches the known spectral sensitivity of opsin from octopus eyes. LACE in isolated preparations suggests that octopus skin is intrinsically light sensitive and that this dispersed light sense might contribute to their unique and novel patterning abilities. Finally, our data suggest that a common molecular mechanism for light detection in eyes may have been co-opted for light sensing in octopus skin and then used for LACE.

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Section: Discussionmentioning

confidence: 89%

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

Ramirez

Oakley

2015

Journal of Experimental Biology

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“…Surprisingly, when we compared this set of transcripts with the recently identified auditory gene set consisting of 274 genes, we found a significant overlap of 58 genes (representation factor 2.5, P < 7.661e-11; Table S1) (21). This observation further suggested that hearing might play a prominent role in Drosophila aggression.…”

Section: Functional and Genetic Disruption Of The Sound-sensitive Ab mentioning

confidence: 85%

“…From the overlapping genes, we selected a cohort of signal transduction genes with reported hearing defects for further analyses: the transient receptor potential (TRP) channel genes nan (nanchung), iav (inactive), and trpl (transient receptor potential-like) and the Ca 2+ signaling-related genes Arr2 (arrestin 2) and inaD (inactivation no afterpotential D) (21). We also added the TRPN gene nompC (no mechanoreceptor potential C), which was identified in neither dataset but is crucial for Drosophila auditory receptor function (22).…”

Section: Functional and Genetic Disruption Of The Sound-sensitive Ab mentioning

confidence: 99%

“…We also added the TRPN gene nompC (no mechanoreceptor potential C), which was identified in neither dataset but is crucial for Drosophila auditory receptor function (22). Flies with mutations in these genes, caused by point mutations or P-element transposons, all displayed abnormal receiver displacement and altered sound-evoked compound action potentials recorded from the antennal nerve (21).…”

Section: Functional and Genetic Disruption Of The Sound-sensitive Ab mentioning

confidence: 99%

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Hearing regulates Drosophila aggression

Versteven

Broeck

Geurten

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Aggression is a universal social behavior important for the acquisition of food, mates, territory, and social status. Aggression in Drosophila is context-dependent and can thus be expected to involve inputs from multiple sensory modalities. Here, we use mechanical disruption and genetic approaches in Drosophila melanogaster to identify hearing as an important sensory modality in the context of intermale aggressive behavior. We demonstrate that neuronal silencing and targeted knockdown of hearing genes in the fly's auditory organ elicit abnormal aggression. Further, we show that exposure to courtship or aggression song has opposite effects on aggression. Our data define the importance of hearing in the control of Drosophila intermale aggression and open perspectives to decipher how hearing and other sensory modalities are integrated at the neural circuit level.A ggression is one of the most important social behaviors in nature, ensuring reproduction and survival when competing for food, territory, or mating partners (1). Aggression is a complex behavior shaped by many factors, including a complex genetic architecture, the integration of various neurotransmitter and hormone systems, and a range of environmental factors (2).Correct integration and processing of sensory information are crucial to evoke an appropriate behavioral response. Previous studies have implicated different sensory modalities in the regulation of aggressive behavior in Drosophila melanogaster, including the olfactory, gustatory, and visual systems (3-6).Another important sensory modality in Drosophila is hearing. Stereotypic sound patterns generated by wing vibration and their behavioral significance have been extensively studied in the context of Drosophila courtship (7-12). On the contrary, nothing is known about the impact of hearing on aggressive behavior. Furthermore, although agonistic sound pulses are known to be generated during aggressive encounters, it is unknown whether they serve as acoustic communication signals to modulate behavior (13).The Drosophila auditory organ, Johnston's organ (JO), is situated in the fly's antenna (Fig. 1A) (14-17). Antennal displacement leads to activation of ∼500 chordotonal stretch-receptor neurons in the JO, which contains AB neurons responsive to sound-evoked vibrations and CE neurons sensitive to sustained antennal deflections caused by gravity and wind (Fig. 1A) (18). The sensory neuron subclasses each innervates a particular region of the antennal mechanosensory and motor center (AMMC), the primary processing center for auditory input in the fly brain (18).In this study, we use mechanical disruption and genetic approaches in D. melanogaster to identify hearing as an important sensory modality in the context of intermale aggressive behavior. We show that neuronal silencing and targeted knockdown of hearing genes in the fly's auditory organ induce abnormal aggression. Further, we show that exposure to courtship or aggression song has opposite effects on aggression. Our data provide evidence on the r...

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“…The ortholog of a key gene in the rhodopsin biosynthesis pathway santa-maria, Dvir\GJ17608, was up-regulated in both species in response to cold acclimation. Rhodopsin has long been known to be the primary pigment for phototransduction (see Katz and Minke (2009) for a review), however recently it has been shown that the rhodopsin signalling pathway also has a several additional lightindependent roles including hearing (Senthilan et al, 2012) and thermosensory signalling (Shen et al, 2011). Shen et al (2011) showed that by knocking out santa-maria in D. melanogaster, flies were unable to discriminate between differences in temperature.…”

Section: Functional Processesmentioning

confidence: 99%

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

et al. 2015

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For many organisms the ability to cold acclimate with the onset of seasonal cold has major implications for their fitness. In insects, where this ability is widespread, the physiological changes associated with increased cold tolerance have been well studied. Despite this, little work has been done to trace changes in gene expression during cold acclimation that lead to an increase in cold tolerance. We used an RNA-Seq approach to investigate this in two species of the Drosophila virilis group. We found that the majority of genes that are differentially expressed during cold acclimation differ between the two species. Despite this, the biological processes associated with the differentially expressed genes were broadly similar in the two species. These included: metabolism, cell membrane composition, and circadian rhythms, which are largely consistent with previous work on cold acclimation/cold tolerance. In addition, we also found evidence of the involvement of the rhodopsin pathway in cold acclimation, a pathway that has been recently linked to thermotaxis. Interestingly, we found no evidence of differential expression of stress genes implying that long-term cold acclimation and short-term stress response may have a different physiological basis.

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Drosophila Auditory Organ Genes and Genetic Hearing Defects

Cited by 200 publications

References 97 publications

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

Eye-independent, light-activated chromatophore expansion (LACE) and expression of phototransduction genes in the skin of Octopus bimaculoides

Hearing regulates Drosophila aggression

How consistent are the transcriptome changes associated with cold acclimation in two species of the Drosophila virilis group?

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