Molecular reconstruction of recurrent evolutionary switching in olfactory receptor specificity.
D. melanogaster
Drosophila sechellia
evolutionary biology
ligand-binding
mutation
neurophysiology
neuroscience
olfactory receptor
parallel evolution
Journal
eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614
Informations de publication
Date de publication:
22 10 2021
22 10 2021
Historique:
received:
24
04
2021
accepted:
21
10
2021
pubmed:
23
10
2021
medline:
27
11
2021
entrez:
22
10
2021
Statut:
epublish
Résumé
Olfactory receptor repertoires exhibit remarkable functional diversity, but how these proteins have evolved is poorly understood. Through analysis of extant and ancestrally reconstructed drosophilid olfactory receptors from the Ionotropic receptor (Ir) family, we investigated evolution of two organic acid-sensing receptors, Ir75a and Ir75b. Despite their low amino acid identity, we identify a common 'hotspot' in their ligand-binding pocket that has a major effect on changing the specificity of both Irs, as well as at least two distinct functional transitions in Ir75a during evolution. Moreover, we show that odor specificity is refined by changes in additional, receptor-specific sites, including those outside the ligand-binding pocket. Our work reveals how a core, common determinant of ligand-tuning acts within epistatic and allosteric networks of substitutions to lead to functional evolution of olfactory receptors.
Identifiants
pubmed: 34677122
doi: 10.7554/eLife.69732
pii: 69732
pmc: PMC8575457
doi:
pii:
Substances chimiques
Receptors, Odorant
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Arthritis Research UK
ID : FC001594
Pays : United Kingdom
Organisme : Medical Research Council
ID : FC001594
Pays : United Kingdom
Organisme : European Research Council
ID : 615094
Pays : International
Organisme : Wellcome Trust
ID : FC001594
Pays : United Kingdom
Organisme : Cancer Research UK
ID : FC001594
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Informations de copyright
© 2021, Prieto-Godino et al.
Déclaration de conflit d'intérêts
LP, HS, RB No competing interests declared
Références
Neuron. 2017 Feb 8;93(3):661-676.e6
pubmed: 28111079
J Hered. 2010 May-Jun;101(3):325-33
pubmed: 19965911
Biol Lett. 2009 Apr 23;5(2):244-7
pubmed: 19141414
Nature. 2018 Aug;560(7719):447-452
pubmed: 30111839
BMC Biol. 2019 Apr 17;17(1):34
pubmed: 30995910
Nat Neurosci. 2014 Jan;17(1):114-20
pubmed: 24316890
Neuron. 2011 Jan 13;69(1):44-60
pubmed: 21220098
Nature. 2006 Mar 23;440(7083):456-62
pubmed: 16554805
Elife. 2015 Jun 04;4:
pubmed: 26041333
J Chem Ecol. 2010 Jun;36(6):599-607
pubmed: 20437263
PLoS Genet. 2018 Apr 23;14(4):e1007341
pubmed: 29684059
Nat Ecol Evol. 2017 Jan 23;1(2):45
pubmed: 28812623
J Insect Physiol. 2018 Apr;106(Pt 1):13-19
pubmed: 28522417
PLoS Genet. 2010 Aug 19;6(8):e1001064
pubmed: 20808886
Nat Commun. 2016 Sep 15;7:12847
pubmed: 27628687
Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11352-7
pubmed: 19541615
Neuron. 2000 Oct;28(1):165-81
pubmed: 11086992
Sci China Life Sci. 2010 Feb;53(2):257-66
pubmed: 20596836
J Neurosci. 2005 Sep 14;25(37):8359-67
pubmed: 16162917
Nature. 2010 Mar 4;464(7285):66-71
pubmed: 20130575
Cell. 2009 Jan 9;136(1):149-62
pubmed: 19135896
Nature. 2011 Sep 28;478(7368):236-40
pubmed: 21964331
Nature. 2021 Sep;597(7874):126-131
pubmed: 34349260
Insect Biochem Mol Biol. 2013 Sep;43(9):888-97
pubmed: 23459169
Nucleic Acids Res. 2012 Jul;40(Web Server issue):W580-4
pubmed: 22661579
Genetics. 2001 Dec;159(4):1393-404
pubmed: 11779783
Sci Signal. 2009 Mar 03;2(60):ra9
pubmed: 19261596
J Neurosci. 2020 Oct 21;40(43):8367-8385
pubmed: 32994339
Nat Commun. 2016 Jun 13;7:ncomms11855
pubmed: 27292132
Nature. 2021 Aug;596(7873):583-589
pubmed: 34265844
Nature. 2016 Nov 3;539(7627):93-97
pubmed: 27776356
Cell. 2006 Apr 7;125(1):143-60
pubmed: 16615896
Sci Rep. 2016 Jan 18;6:19441
pubmed: 26777264
Elife. 2017 Oct 24;6:
pubmed: 29063835
Bioinformatics. 2017 Sep 1;33(17):2779-2780
pubmed: 28472360
J Neurosci. 2011 Sep 21;31(38):13357-75
pubmed: 21940430
Behav Genet. 1998 Nov;28(6):455-64
pubmed: 9926614
Proteins. 2008 Nov 15;73(3):656-71
pubmed: 18491377
Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14081-6
pubmed: 22891317
Front Mol Neurosci. 2021 Feb 01;13:638839
pubmed: 33597847
Nature. 2020 Mar;579(7799):402-408
pubmed: 32132713
Nat Rev Genet. 2005 Feb;6(2):119-27
pubmed: 15716908
Genome Biol Evol. 2018 Jan 1;10(1):189-206
pubmed: 29228179
PLoS Genet. 2012;8(7):e1002821
pubmed: 22807691
Curr Biol. 2006 Jan 10;16(1):101-9
pubmed: 16401429
Nature. 2006 Nov 16;444(7117):295-301
pubmed: 17108953
Trends Genet. 2010 Jul;26(7):307-16
pubmed: 20537755
Cold Spring Harb Protoc. 2011 Jul 01;2011(7):824-38
pubmed: 21724819
Nature. 2009 Dec 10;462(7274):745-56
pubmed: 19946266
J Agric Food Chem. 2018 Dec 26;66(51):13346-13366
pubmed: 30453735
Mol Biol Evol. 2009 Sep;26(9):2073-86
pubmed: 19542205
Nat Rev Genet. 2008 Nov;9(11):855-67
pubmed: 18852697