Article

The molecular basis for water taste in Drosophila

Department of Molecular and Cell Biology and Helen Wills Neuroscience Institute, CA, USA.
Nature (Impact Factor: 42.35). 04/2010; 465(7294):91-5. DOI: 10.1038/nature09011
Source: PubMed

ABSTRACT The detection of water and the regulation of water intake are essential for animals to maintain proper osmotic homeostasis. Drosophila and other insects have gustatory sensory neurons that mediate the recognition of external water sources, but little is known about the underlying molecular mechanism for water taste detection. Here we identify a member of the degenerin/epithelial sodium channel family, PPK28, as an osmosensitive ion channel that mediates the cellular and behavioural response to water. We use molecular, cellular, calcium imaging and electrophysiological approaches to show that ppk28 is expressed in water-sensing neurons, and that loss of ppk28 abolishes water sensitivity. Moreover, ectopic expression of ppk28 confers water sensitivity to bitter-sensing gustatory neurons in the fly and sensitivity to hypo-osmotic solutions when expressed in heterologous cells. These studies link an osmosensitive ion channel to water taste detection and drinking behaviour, providing the framework for examining the molecular basis for water detection in other animals.

0 Followers
 · 
104 Views
  • [Show abstract] [Hide abstract]
    ABSTRACT: While gustatory sensing of the five primary flavors (sweet, salty, sour, bitter, and savory) has been extensively studied, pathways that detect non-canonical taste stimuli remain relatively unexplored. In particular, while reactive oxygen species cause generalized damage to biological systems, no gustatory mechanism to prevent ingestion of such material has been identified in any organism. We observed that light inhibits C. elegans feeding and used light as a tool to uncover molecular and neural mechanisms for gustation. Light can generate hydrogen peroxide, and we discovered that hydrogen peroxide similarly inhibits feeding. The gustatory receptor family members LITE-1 and GUR-3 are required for the inhibition of feeding by light and hydrogen peroxide. The I2 pharyngeal neurons increase calcium in response to light and hydrogen peroxide, and these responses require GUR-3 and a conserved antioxidant enzyme peroxiredoxin PRDX-2. Our results demonstrate a gustatory mechanism that mediates the detection and blocks ingestion of a non-canonical taste stimulus, hydrogen peroxide. Copyright © 2015 Elsevier Inc. All rights reserved.
    Neuron 01/2015; DOI:10.1016/j.neuron.2014.12.061 · 15.98 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: The gustatory system provides vital sensory information to determine feeding and appetitive learning behaviors. Very little is known, however, about higher-order gustatory circuits in the highly tractable model for neurobiology, Drosophila melanogaster. Here we report second-order sweet gustatory projection neurons (sGPNs) in the Drosophila brain using a powerful behavioral screen. Silencing neuronal activity reduces appetitive behaviors, whereas inducible activation results in food acceptance via proboscis extensions. sGPNs show functional connectivity with Gr5a(+) sweet taste neurons and are activated upon sucrose application to the labellum. By tracing sGPN axons, we identify the antennal mechanosensory and motor center (AMMC) as an immediate higher-order processing center for sweet taste. Interestingly, starvation increases sucrose sensitivity of the sGPNs in the AMMC, suggesting that hunger modulates the responsiveness of the secondary sweet taste relay. Together, our results provide a foundation for studying gustatory processing and its modulation by the internal nutrient state. Copyright © 2015 Elsevier Inc. All rights reserved.
    Neuron 02/2015; 85(4). DOI:10.1016/j.neuron.2015.01.005 · 15.98 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Humidity is one of the most important factors that determines the geographical distribution and survival of terrestrial animals. The ability to detect variation in humidity is conserved across many species. Here, we established a novel behavioral assay that revealed the thirsty Drosophila exhibits strong hygrotactic behavior, and it can locate water by detecting humidity gradient. In addition, exposure to high levels of moisture was sufficient to elicit proboscis extension reflex behavior in thirsty flies. Furthermore, we found that the third antennal segment was necessary for hygrotactic behavior in thirsty flies, while arista was required for the avoidance of moist air in hydrated flies. These results indicated that two types of hygroreceptor cells exist in Drosophila: one located in the third antennal segment that mediates hygrotactic behavior in thirst status, and the other located in arista which is responsible for the aversive behavior toward moist air in hydration status. Using a neural silencing screen, we demonstrated that synaptic output from the mushroom body α/β surface and posterior neurons was required for both hygrotactic behavior and moisture-aversive behavior.
    PLoS ONE 03/2015; 10(3):e0119162. DOI:10.1371/journal.pone.0119162 · 3.53 Impact Factor

Full-text (2 Sources)

Download
12 Downloads
Available from
Aug 13, 2014