The Molecular Basis for Attractive Salt-taste Coding in Drosophila

Overview

Journal Science

Specialty Science

Date 2013 Jun 15

PMID 23766326

Citations 158

Authors

Yali V Zhang

Jinfei Ni

Craig Montell

Affiliations

Soon will be listed here.

Abstract

Below a certain level, table salt (NaCl) is beneficial for animals, whereas excessive salt is harmful. However, it remains unclear how low- and high-salt taste perceptions are differentially encoded. We identified a salt-taste coding mechanism in Drosophila melanogaster. Flies use distinct types of gustatory receptor neurons (GRNs) to respond to different concentrations of salt. We demonstrated that a member of the newly discovered ionotropic glutamate receptor (IR) family, IR76b, functioned in the detection of low salt and was a Na(+) channel. The loss of IR76b selectively impaired the attractive pathway, leaving salt-aversive GRNs unaffected. Consequently, low salt became aversive. Our work demonstrated that the opposing behavioral responses to low and high salt were determined largely by an elegant bimodal switch system operating in GRNs.

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References

Weiss L, Dahanukar A, Kwon J, Banerjee D, Carlson J . The molecular and cellular basis of bitter taste in Drosophila. Neuron. 2011; 69(2):258-72. PMC: 3033050. DOI: 10.1016/j.neuron.2011.01.001. View

Benton R, Vannice K, Gomez-Diaz C, Vosshall L . Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 2009; 136(1):149-62. PMC: 2709536. DOI: 10.1016/j.cell.2008.12.001. View

Lu B, Su Y, Das S, Liu J, Xia J, Ren D . The neuronal channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell. 2007; 129(2):371-83. DOI: 10.1016/j.cell.2007.02.041. View

Hiroi M, Meunier N, Marion-Poll F, Tanimura T . Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J Neurobiol. 2004; 61(3):333-42. DOI: 10.1002/neu.20063. View

Wang Z, Singhvi A, Kong P, Scott K . Taste representations in the Drosophila brain. Cell. 2004; 117(7):981-91. DOI: 10.1016/j.cell.2004.06.011. View

Liu L, Leonard A, Motto D, Feller M, Price M, Johnson W . Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron. 2003; 39(1):133-46. DOI: 10.1016/s0896-6273(03)00394-5. View

Balakrishnan R, Rodrigues V . The shaker and shaking-B genes specify elements in the processing of gustatory information in Drosophila melanogaster. J Exp Biol. 1991; 157:161-81. DOI: 10.1242/jeb.157.1.161. View

Cameron P, Hiroi M, Ngai J, Scott K . The molecular basis for water taste in Drosophila. Nature. 2010; 465(7294):91-5. PMC: 2865571. DOI: 10.1038/nature09011. View

Croset V, Rytz R, Cummins S, Budd A, Brawand D, Kaessmann H . Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet. 2010; 6(8):e1001064. PMC: 2924276. DOI: 10.1371/journal.pgen.1001064. View

10.

Chandrashekar J, Kuhn C, Oka Y, Yarmolinsky D, Hummler E, Ryba N . The cells and peripheral representation of sodium taste in mice. Nature. 2010; 464(7286):297-301. PMC: 2849629. DOI: 10.1038/nature08783. View

11.

Nakamura M, Baldwin D, Hannaford S, Palka J, Montell C . Defective proboscis extension response (DPR), a member of the Ig superfamily required for the gustatory response to salt. J Neurosci. 2002; 22(9):3463-72. PMC: 6758379. DOI: 20026336. View

12.

Thorne N, Chromey C, Bray S, Amrein H . Taste perception and coding in Drosophila. Curr Biol. 2004; 14(12):1065-79. DOI: 10.1016/j.cub.2004.05.019. View

13.

Potter C, Tasic B, Russler E, Liang L, Luo L . The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell. 2010; 141(3):536-48. PMC: 2883883. DOI: 10.1016/j.cell.2010.02.025. View

14.

Vosshall L, Stocker R . Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci. 2007; 30:505-33. DOI: 10.1146/annurev.neuro.30.051606.094306. View

15.

DeSimone J, Heck G, DeSimone S . Active ion transport in dog tongue: a possible role in taste. Science. 1981; 214(4524):1039-41. DOI: 10.1126/science.7302576. View

16.

Meunier N, Marion-Poll F, Rospars J, Tanimura T . Peripheral coding of bitter taste in Drosophila. J Neurobiol. 2003; 56(2):139-52. DOI: 10.1002/neu.10235. View

17.

Abuin L, Bargeton B, Ulbrich M, Isacoff E, Kellenberger S, Benton R . Functional architecture of olfactory ionotropic glutamate receptors. Neuron. 2011; 69(1):44-60. PMC: 3050028. DOI: 10.1016/j.neuron.2010.11.042. View

18.

Zuo J, De Jager P, Takahashi K, Jiang W, Linden D, Heintz N . Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature. 1997; 388(6644):769-73. DOI: 10.1038/42009. View

19.

Montell C . A taste of the Drosophila gustatory receptors. Curr Opin Neurobiol. 2009; 19(4):345-53. PMC: 2747619. DOI: 10.1016/j.conb.2009.07.001. View

20.

Hodgson E, LETTVIN J, ROEDER K . Physiology of a primary chemoreceptor unit. Science. 1955; 122(3166):417-8. DOI: 10.1126/science.122.3166.417-a. View