Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction.
Ionotropic glutamate receptors (iGluRs) are a highly conserved family of ligand-gated ion channels present in animals, plants, and bacteria, which are best characterized for their roles in synaptic communication in vertebrate nervous systems. A variant subfamily of iGluRs, the Ionotropic Receptors (IRs), was recently identified as a new class of olfactory receptors in the fruit fly, Drosophila melanogaster, hinting at a broader function of this ion channel family in detection of environmental, as well as intercellular, chemical signals. Here, we investigate the origin and evolution of IRs by comprehensive evolutionary genomics and in situ expression analysis. In marked contrast to the insect-specific Odorant Receptor family, we show that IRs are expressed in olfactory organs across Protostomia--a major branch of the animal kingdom that encompasses arthropods, nematodes, and molluscs--indicating that they represent an ancestral protostome chemosensory receptor family. Two subfamilies of IRs are distinguished: conserved "antennal IRs," which likely define the first olfactory receptor family of insects, and species-specific "divergent IRs," which are expressed in peripheral and internal gustatory neurons, implicating this family in taste and food assessment. Comparative analysis of drosophilid IRs reveals the selective forces that have shaped the repertoires in flies with distinct chemosensory preferences. Examination of IR gene structure and genomic distribution suggests both non-allelic homologous recombination and retroposition contributed to the expansion of this multigene family. Together, these findings lay a foundation for functional analysis of these receptors in both neurobiological and evolutionary studies. Furthermore, this work identifies novel targets for manipulating chemosensory-driven behaviours of agricultural pests and disease vectors.
Croset
Vincent
V
Center for Integrative Genomics, University of Lausanne, Lausanne, Switzerland.
Rytz
Raphael
R
Cummins
Scott F
SF
Budd
Aidan
A
Brawand
David
D
Kaessmann
Henrik
H
Gibson
Toby J
TJ
Benton
Richard
R
D000818:Animals; D004330:Drosophila / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D019476:Insect Proteins / Q000235:genetics* / Q000378:metabolism; D007313:Insecta / Q000145:classification / Q000235:genetics* / Q000502:physiology; D007448:Invertebrates / Q000145:classification / Q000235:genetics / Q000502:physiology; D008969:Molecular Sequence Data; D005810:Multigene Family; D010802:Phylogeny; D058468:Receptors, Ionotropic Glutamate / Q000235:genetics* / Q000378:metabolism; D018035:Receptors, Odorant / Q000235:genetics / Q000378:metabolism; D012903:Smell; D013649:Taste
D019476:Insect Proteins; D058468:Receptors, Ionotropic Glutamate; D018035:Receptors, Odorant
Mol Biol Evol. 1995 May;12(3):391-404
7739381
Curr Biol. 2005 Feb 22;15(4):R119-21
15723778
Proc Natl Acad Sci U S A. 2003 Nov 25;100 Suppl 2:14537-42
14608037
Nat Genet. 2008 Apr;40(4):476-83
18311141
Curr Opin Neurobiol. 2009 Aug;19(4):345-53
19660932
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
15034147
Nat Rev Genet. 2009 Jan;10(1):19-31
19030023
Cell Mol Life Sci. 2006 Jul;63(14):1579-85
16786219
J Exp Biol. 2002 Apr;205(Pt 7):877-96
11916985
Neuron. 1999 Mar;22(3):451-61
10197526
Comput Appl Biosci. 1993 Dec;9(6):745-56
8143162
Mol Biol Evol. 2007 Dec;24(12):2842-50
17965454
Annu Rev Microbiol. 2001;55:709-42
11544372
Brain Res. 1997 Oct 17;771(2):292-304
9401750
EMBO J. 2009 Jun 17;28(12):1812-23
19461580
Curr Opin Neurobiol. 1999 Oct;9(5):634-9
10508748
Neurosci Behav Physiol. 2009 Oct;39(8):763-73
19779829
J Neurosci. 2004 Sep 29;24(39):8522-30
15456826
Mol Biol Evol. 2004 Jan;21(1):36-44
12949132
Nat Rev Neurosci. 2010 Mar;11(3):212-7
20029439
J Neurosci. 2005 Sep 14;25(37):8359-67
16162917
J Mol Biol. 2004 Jul 16;340(4):783-95
15223320
Genome Res. 2004 May;14(5):988-95
15123596
Nat Rev Neurosci. 2009 Aug;10(8):611-8
19584894
J Neurosci. 2001 Mar 1;21(5):1510-22
11222641
Heredity (Edinb). 2009 Sep;103(3):208-16
19436326
Nature. 1998 Nov 12;396(6707):125-6
9823891
BMC Evol Biol. 2009 Apr 21;9:79
19383158
Cell. 2009 Jan 9;136(1):149-62
19135896
Genetics. 2007 Nov;177(3):1395-416
18039874
PLoS One. 2008 Jun 18;3(6):e2442
18560591
Nature. 1998 Oct 29;395(6705):913-7
9804426
BMC Biol. 2009 Jun 24;7:34
19552814
Genome Res. 2005 Feb;15(2):330-40
15687296
Genome Res. 2005 Aug;15(8):1153-60
16077014
Bioinformatics. 2005 May 1;21(9):2104-5
15647292
EMBO J. 2002 May 15;21(10):2312-22
12006484
Cell. 2006 Dec 29;127(7):1453-67
17190607
Neuropharmacology. 2009 Jan;56(1):2-5
18655795
Annu Rev Neurosci. 2007;30:505-33
17506643
Neuron. 2000 Apr;26(1):35-43
10798390
PLoS Biol. 2008 Mar 18;6(3):e63
18351802
Nature. 2007 Nov 8;450(7167):203-18
17994087
Science. 2000 Mar 10;287(5459):1830-4
10710312
Bioinformatics. 2007 Jan 1;23(1):127-8
17050570
Plant Physiol. 2006 Nov;142(3):963-71
17012403
Annu Rev Genet. 2005;39:121-52
16285855
Annu Rev Physiol. 2004;66:161-81
14977400
Mol Biol Evol. 1998 Nov;15(11):1562-7
12572619
Syst Biol. 2003 Oct;52(5):696-704
14530136
Genome Res. 2005 Jan;15(1):1-18
15632085
J Comp Neurol. 2003 Jan 1;455(1):125-38
12455001
Nucleic Acids Res. 2008 Jan;36(Database issue):D281-8
18039703
Neuron. 2004 Sep 2;43(5):703-14
15339651
J Comp Physiol Psychol. 1973 Mar;82(3):368-81
4706579
Bioinformatics. 2006 Dec 1;22(23):2971-2
17021158
Bioinformatics. 2009 May 1;25(9):1189-91
19151095
Comput Appl Biosci. 1997 Oct;13(5):555-6
9367129
PLoS Biol. 2008 Aug 5;6(8):e198
18687026
Bioinformatics. 1998;14(9):755-63
9918945
PLoS Biol. 2007 Feb;5(2):e14
17298171
Cell. 2001 Mar 9;104(5):661-73
11257221
PLoS Biol. 2006 Feb;4(2):e20
16402857
Nat Rev Genet. 2008 Dec;9(12):951-63
19002141
Genome Biol. 2007;8(11):R235
18039354
J Mol Biol. 2001 Jan 19;305(3):567-80
11152613
Nature. 2009 Dec 24;462(7276):1061-4
19956092
BMC Biol. 2009 Jun 04;7:28
19493360
Nucleic Acids Res. 2003 Feb 1;31(3):1033-7
12560500
Development. 1993 Jun;118(2):401-15
8223268
Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3312-7
17360644
Syst Biol. 2001 Sep-Oct;50(5):676-88
12116938
Bioinformatics. 2005 Feb 15;21(4):456-63
15608047
Bioinformatics. 2006 May 15;22(10):1269-71
16543274
Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):299-325
8805
Mol Biol Evol. 2002 Jul;19(7):1066-82
12082126
Chem Senses. 2004 Mar;29(3):179-87
15047592
Genetics. 2008 Jul;179(3):1601-55
18622037
Ann N Y Acad Sci. 2009 Jul;1170:468-75
19686179
Mol Biol Evol. 1999 Jun;16(6):826-38
10368960
Micron. 2009 Jul-Aug;40(5-6):571-6
19428262
J Gen Physiol. 1970 Dec;56(6):768-82
5483106
PLoS One. 2007 Jun 06;2(6):e506
17551586
J Exp Biol. 2009 Jul;212(Pt 13):2037-44
19525430
Nature. 2009 Dec 10;462(7274):745-56
19946266
Genetica. 2005 Feb;123(1-2):137-45
15881686
Trends Neurosci. 2003 Jan;26(1):27-32
12495860
Genetics. 2007 Nov;177(3):1269-76
18039866
Mol Biol Evol. 2002 May;19(5):748-61
11961108
Nature. 1999 Dec 16;402(6763):817-21
10617203