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The molecular basis for water taste in Drosophila

Abstract

The detection of water and the regulation of water intake are essential for animals to maintain proper osmotic homeostasis1. Drosophila and other insects have gustatory sensory neurons that mediate the recognition of external water sources2,3,4, but little is known about the underlying molecular mechanism for water taste detection. Here we identify a member of the degenerin/epithelial sodium channel family5, 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.

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Figure 1: ppk28-Gal4 labels neurons that respond to water.
Figure 2: The ppk28 gene is necessary for cellular and behavioural water responses.
Figure 3: Ectopic expression of ppk28 confers water sensitivity.
Figure 4: Heterologous cells expressing PPK28 respond to hypo-osmolarity.

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Acknowledgements

We thank K. Vranizan for assistance with microarray analyses. K. Gerhold and D. Bautista provided the TRPV4 construct, protocols and advice for HEK293 experiments; the Roelink laboratory provided tissue culture facilities and advice. G. Agarwaal generated heat map images in Matlab for data presentation. W. Fischler generated the NP1017 G-CaMP data in Supplementary Information. We are grateful to C. Zuker and members of the Scott laboratory for comments on the manuscript. This work was supported by a grant from the NIH (NIDCD), a Burroughs-Wellcome CAREER Award and a John Merck Award to K.S. and a NIH predoctoral fellowship to P.C. K.S. is an HHMI Early Career Scientist.

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P.C. performed most experiments and co-wrote the manuscript. M.H. performed the electrophysiological recordings and the HEK293 heterologous experiments. J.N. provided expertise on the microarray experiments. K.S. co-wrote the manuscript and supervised the project.

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Correspondence to Kristin Scott.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures S1-S6 with legends and Supplementary Table S1. (PDF 8415 kb)

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Cameron, P., Hiroi, M., Ngai, J. et al. The molecular basis for water taste in Drosophila. Nature 465, 91–95 (2010). https://doi.org/10.1038/nature09011

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