The molecular and cellular basis of bitter taste in Drosophila.
The extent of diversity among bitter-sensing neurons is a fundamental issue in the field of taste. Data are limited and conflicting as to whether bitter neurons are broadly tuned and uniform, resulting in indiscriminate avoidance of bitter stimuli, or diverse, allowing a more discerning evaluation of food sources. We provide a systematic analysis of how bitter taste is encoded by the major taste organ of the Drosophila head, the labellum. Each of 16 bitter compounds is tested physiologically against all 31 taste hairs, revealing responses that are diverse in magnitude and dynamics. Four functional classes of bitter neurons are defined. Four corresponding classes are defined through expression analysis of all 68 gustatory taste receptors. A receptor-to-neuron-to-tastant map is constructed. Misexpression of one receptor confers bitter responses as predicted by the map. These results reveal a degree of complexity that greatly expands the capacity of the system to encode bitter taste.
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06520-8103, USA.
Linnea A
LA
Weiss
Anupama
A
Dahanukar
Jae Young
JY
Kwon
Diya
D
Banerjee
John R
JR
Carlson
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D030801:Animals, Genetically Modified; D001522:Behavior, Animal; D002755:Choice Behavior; D029721:Drosophila Proteins / Q000502:physiology; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000502:physiology*; D008024:Ligands; D008297:Male; D009475:Neurons, Afferent / Q000145:classification / Q000502:physiology*; D011956:Receptors, Cell Surface / Q000502:physiology; D058618:Sensilla / Q000166:cytology / Q000502:physiology; D013649:Taste / Q000502:physiology*; D013652:Taste Threshold / Q000502:physiology
D029721:Drosophila Proteins; D008024:Ligands; D011956:Receptors, Cell Surface; C405956:gustatory receptor, Drosophila
Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14526-30
14523229
Nature. 2005 Mar 10;434(7030):225-9
15759003
WormBook. 2006 Oct 25;:1-29
18050433
Nature. 2008 Mar 27;452(7186):473-7
18305480
PLoS Biol. 2008 May 27;6(5):e125
18846726
Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14833-8
20679196
Cell. 2003 Oct 31;115(3):255-66
14636554
Cell. 2001 Aug 10;106(3):381-90
11509186
Phytochemistry. 2003 Mar;62(6):837-49
12590111
Cell. 2009 Oct 16;139(2):234-44
19837029
Genetics. 2010 Sep;186(1):79-95
20551440
Curr Biol. 2008 Nov 25;18(22):1797-801
19026541
Neuron. 2006 Jan 19;49(2):285-95
16423701
Neuron. 2007 Feb 1;53(3):353-69
17270733
Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14537-42
14608037
J Neurosci. 2005 Sep 14;25(37):8359-67
16162917
Physiol Genomics. 2005 Jul 14;22(2):139-49
15886333
Curr Biol. 2001 Jun 5;11(11):822-35
11516643
Neuron. 2008 Jul 10;59(1):110-24
18614033
J Neurosci. 2003 Oct 29;23(30):9906-12
14586020
Annu Rev Neurosci. 2006;29:163-201
16776583
J Neurosci. 1999 Jun 1;19(11):4520-32
10341252
J Neurosci. 2009 Oct 14;29(41):12940-7
19828808
Nature. 2007 Mar 29;446(7135):542-6
17392786
Vet Hum Toxicol. 1993 Jun;35(3):234-6
8351798
Curr Biol. 2004 Jun 22;14(12):1065-79
15202999
Zoolog Sci. 2002 Sep;19(9):1009-18
12362054
Cell Tissue Res. 1994 Jan;275(1):3-26
8118845
Curr Biol. 2009 Oct 13;19(19):1623-7
19765987
Curr Biol. 2007 Apr 3;17(7):606-12
17363256
Nature. 2008 Apr 24;452(7190):1007-11
18408711
Nat Neurosci. 2001 May;4(5):492-8
11319557
Science. 2000 Mar 10;287(5459):1830-4
10710312
J Neurosci. 2006 Aug 30;26(35):8900-8
16943545
J Comp Neurol. 2008 Feb 1;506(4):548-68
18067151
Curr Biol. 2007 Oct 23;17(20):1809-16
17919910
J Neurobiol. 2004 Dec;61(3):333-42
15389687
J Comp Neurol. 2010 Oct 15;518(20):4147-81
20878781
Proc Natl Acad Sci U S A. 2010 May 4;107(18):8440-5
20404155
Curr Biol. 2010 Jan 12;20(1):1-8
20036540
J Neurobiol. 2003 Aug;56(2):139-52
12838579
Invert Neurosci. 1997 Sep-Dec;3(2-3):127-35
9783438
Cell Tissue Res. 1981;216(3):513-23
6786751
J Neurosci. 2010 Apr 7;30(14):5028-36
20371823
Cell. 2004 Jun 25;117(7):981-91
15210117
Cell. 2001 Mar 9;104(5):661-73
11257221
PLoS Biol. 2006 Feb;4(2):e20
16402857
SEB Exp Biol Ser. 2009;63:1-38
19174987
Nature. 2007 Jan 4;445(7123):86-90
17167414
Sci Am. 1989 Feb;260(2):42-9
2643825
Cell. 2000 Mar 17;100(6):693-702
10761934
Neuron. 2001 May;30(2):537-52
11395013
J Neurosci. 2008 Jul 9;28(28):7121-9
18614681
Development. 1993 Jun;118(2):401-15
8223268
Science. 2008 Mar 21;319(5870):1679-83
18356529
Chem Senses. 2003 May;28(4):301-13
12771017
Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3574-8
17360684
J Neurosci. 2002 Aug 15;22(16):7281-7
12177223
Neuron. 2010 Aug 26;67(4):555-61
20797533
Physiol Behav. 1994 Dec;56(6):1217-27
7878094
Curr Biol. 2006 Sep 19;16(18):1812-7
16979558
J Morphol. 1976 Oct;150(2):327-341
30261703
PLoS Biol. 2009 Jun 30;7(6):e1000147
19564899
Nature. 2008 Apr 24;452(7190):1002-6
18408712
PLoS One. 2009;4(3):e4796
19274098
Genetics. 1988 Jun;119(2):399-406
17246428
Science. 1955 Sep 2;122(3166):417-8
13246649
Neuron. 1999 Feb;22(2):339-47
10069339
Neuron. 2007 Nov 8;56(3):503-16
17988633
Cell Tissue Res. 2001 Jun;304(3):423-37
11456419
Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4495-500
19246397
Cell. 2009 Oct 2;139(1):45-59
19804753