Antennal Transcriptome Screening and Identification of Chemosensory Proteins in the Double-Spine European Spruce Bark Beetle, Ips duplicatus (Coleoptera: Scolytinae)
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
Johny Jibin 43950/1312/3175
Internal Grant Agency, FFWS, CZU, Prague
CZ.02.1.01/0.0/0.0/15_003/0000433
EXTEMIT-K
2023-24
Excellent Team Grant
PubMed
39273461
PubMed Central
PMC11395090
DOI
10.3390/ijms25179513
PII: ijms25179513
Knihovny.cz E-resources
- Keywords
- Coleoptera, Ips duplicatus, RNAseq, antennal transcriptome, bark beetles, chemosensory proteins, olfaction, orthologs, tetramer OBP,
- MeSH
- Coleoptera * genetics metabolism MeSH
- Phylogeny * MeSH
- Insect Proteins * genetics metabolism MeSH
- Receptors, Odorant * genetics metabolism MeSH
- Gene Expression Profiling methods MeSH
- Transcriptome * MeSH
- Arthropod Antennae * metabolism MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Insect Proteins * MeSH
- odorant-binding protein MeSH Browser
- Receptors, Odorant * MeSH
The northern bark beetle, Ips duplicatus, is an emerging economic pest, reportedly infesting various species of spruce (Picea spp.), pine (Pinus spp.), and larch (Larix spp.) in Central Europe. Recent climate changes and inconsistent forest management practices have led to the rapid spread of this species, leaving the current monitoring strategies inefficient. As understanding the molecular components of pheromone detection is key to developing novel control strategies, we generated antennal transcriptomes from males and females of this species and annotated the chemosensory proteins. We identified putative candidates for 69 odorant receptors (ORs), 50 ionotropic receptors (IRs), 25 gustatory receptors (GRs), 27 odorant-binding proteins (OBPs), including a tetramer-OBP, 9 chemosensory proteins (CSPs), and 6 sensory neuron membrane proteins (SNMPs). However, no sex-specific chemosensory genes were detected. The phylogenetic analysis revealed conserved orthology in bark beetle chemosensory proteins, especially with a major forest pest and co-habitant, Ips typographus. Recent large-scale functional studies in I. typographus chemoreceptors add greater significance to the orthologous sequences reported here. Nevertheless, identifying chemosensory genes in I. duplicatus is valuable to understanding the chemosensory system and its evolution in bark beetles (Coleoptera) and, generally, insects.
See more in PubMed
Wermelinger B., Mathis D.S., Knížek M., Forster B. Tracking the Spread of the Northern Bark Beetle (Ips duplicatus [Sahlb.]) in Europe and First Records from Switzerland and Liechtenstein. Alp. Entomol. 2020;4:179–184. doi: 10.3897/alpento.4.53808. DOI
Jeger M., Bragard C., Caffier D., Candresse T., Chatzivassiliou E., Dehnen-Schmutz K., Gilioli G., Jaques Miret J.A., MacLeod A., Navajas Navarro M., et al. Pest Categorisation of Ips duplicatus. EFSA J. 2017;15:e05040. doi: 10.2903/j.efsa.2017.5040. PubMed DOI PMC
Davídková M., Kleinová L., Doležal P. Overwintering Migration of the Double-Spined Spruce Bark Beetle Ips duplicatus (Sahlberg, 1836) (Coleoptera; Curculionidae) Forests. 2023;14:131. doi: 10.3390/f14010131. DOI
Holuša J., Lukášová K., Lubojacký J. Comparison of Seasonal Flight Activity of Ips typographus and Ips duplicatus. Sci. Agric. Bohem. 2012;2012:109–115.
Zimová S., Resnerová K., Vanická H., Horák J., Trombik J., Kacprzyk M., Lindelöw Å., Duduman M.L., Holuša J. Infection Levels of the Microsporidium Larssoniella duplicati in Populations of the Invasive Bark Beetle Ips duplicatus: From Native to New Outbreak Areas. Forests. 2019;10:131. doi: 10.3390/f10020131. DOI
Holusa J., Lubojacky J., Knizek M. Distribution of the Double-Spined Spruce Bark Beetle Ips duplicatus in the Czech Republic: Spreading in 1997–2009. Phytoparasitica. 2010;38:435–443. doi: 10.1007/s12600-010-0121-9. DOI
Kavčič A., Devetak Z., Piškur B., Groznik E., De Groot M. First Record of the Northern Spruce Bark Beetle, Ips duplicatus (Sahlberg, 1836), in Slovenia. BioInvasions Rec. 2023;12:699–710. doi: 10.3391/bir.2023.12.3.07. DOI
Toth D., Maitah M., Maitah K., Jarolínová V. The Impacts of Calamity Logging on the Development of Spruce Wood Prices in Czech Forestry. Forests. 2020;11:283. doi: 10.3390/f11030283. DOI
Duduman M.L., Beránková K., Jakuš R., Hradecký J., Jirošová A. Efficiency and Sustainability of Ips duplicatus (Coleoptera: Curculionidae) Pheromone Dispensers with Different Designs. Forests. 2022;13:511. doi: 10.3390/f13040511. DOI
Holuša J., Grodzki W., Lukašová K., Lubojacký J. Pheromone Trapping of the Double-Spined Bark Beetle Ips duplicatus (Coleoptera: Curculionidae, Scolytinae): Seasonal Variation in Abundance. Folia For. Pol. Ser. A. 2013;55:3–9. doi: 10.2478/ffp-2013-0001. DOI
Byers J.A., Schlyter F., Birgersson G., Francke W. E-Myrcenol In Ips duplicatus: An Aggregation Pheromone Component New for Bark Beetles. Experientia. 1990;46:1209–1211. doi: 10.1007/BF01936939. DOI
Schlyter F., Birgersson G., Byers J.A., Bakke A. The Aggregation Pheromone of Ips duplicatus and Its Role in Competitive Interactions with I. typographus (Coleoptera: Scolytidae) Chemoecology. 1992;3:103–112. doi: 10.1007/BF01370137. DOI
Schlyter F., Zhang Q.H., Liu G.T., Ji L.Z. A Successful Case of Pheromone Mass Trapping of the Bark Beetle Ips duplicatus in a Forest Island, Analysed by 20-Year Time-Series Data. Integr. Pest. Manag. Rev. 2001;6:185–196. doi: 10.1023/A:1025767217376. DOI
Zhang Q.-H., Schlyter F., Liu G.-T., Sheng M.-L., Birgersson G. Electrophysiological and Behavioral Responses of Ips duplicatus to Aggregation Pheromone in Inner Mongolia, China: Amitinol as a Potential Pheromone Component. J. Chem. Ecol. 2007;33:1303–1315. doi: 10.1007/s10886-007-9320-3. PubMed DOI
Duduman M.L. Field Response of the Northern Spruce Bark Beetle Ips duplicatus (Sahlberg) (Coleoptera: Curculionidae, Scolytinae) to Different Combinations of Synthetic Pheromone with (−)-α-Pinene and (+)-Limonene. Agric. For. Entomol. 2014;16:102–109. doi: 10.1111/afe.12039. DOI
Šotola V., Holuša J., Kuželka K., Kula E. Felled and Lure Trap Trees with Uncut Branches Are Only Weakly Attractive to the Double-Spined Bark Beetle, Ips duplicatus. Forests. 2021;12:941. doi: 10.3390/f12070941. DOI
Hansson B.S., Stensmyr M.C. Evolution of Insect Olfaction. Neuron. 2011;72:698–711. doi: 10.1016/j.neuron.2011.11.003. PubMed DOI
de Bruyne M., Baker T.C. Odor Detection in Insects: Volatile Codes. J. Chem. Ecol. 2008;34:882–897. doi: 10.1007/s10886-008-9485-4. PubMed DOI
Clyne P.J., Warr C.G., Freeman M.R., Lessing D., Kim J., Carlson J.R. A Novel Family of Divergent Seven-Transmembrane Proteins: Candidate Odorant Receptors in Drosophila. Neuron. 1999;22:327–338. doi: 10.1016/S0896-6273(00)81093-4. PubMed DOI
Gao Q., Chess A. Identification of Candidate Drosophila Olfactory Receptors from Genomic DNA Sequence. Genomics. 1999;60:31–39. doi: 10.1006/geno.1999.5894. PubMed DOI
Vosshall L.B., Stocker R.F. Molecular Architecture of Smell and Taste in Drosophila. Annu. Rev. Neurosci. 2007;30:505–533. doi: 10.1146/annurev.neuro.30.051606.094306. PubMed DOI
Benton R., Vannice K.S., Vosshall L.B. An Essential Role for a CD36-Related Receptor in Pheromone Detection in Drosophila. Nature. 2007;450:289–293. doi: 10.1038/nature06328. PubMed DOI
Benton R., Vannice K.S., Gomez-Diaz C., Vosshall L.B. Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila. Cell. 2009;136:149–162. doi: 10.1016/j.cell.2008.12.001. PubMed DOI PMC
Scalzotto M., Ng R., Cruchet S., Saina M., Armida J., Su C.Y., Benton R. Pheromone Sensing in Drosophila Requires Support Cell-Expressed Osiris 8. BMC Biol. 2022;20:1–18. doi: 10.1186/s12915-022-01425-w. PubMed DOI PMC
Robertson H.M. The Insect Chemoreceptor Superfamily Is Ancient in Animals. Chem. Senses. 2015;40:609–614. doi: 10.1093/chemse/bjv046. PubMed DOI
Thoma M., Missbach C., Jordan M.D., Grosse-Wilde E., Newcomb R.D., Hansson B.S. Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family. Front. Ecol. Evol. 2019;7:281. doi: 10.3389/fevo.2019.00281. DOI
del Mármol J., Yedlin M.A., Ruta V. The Structural Basis of Odorant Recognition in Insect Olfactory Receptors. Nature. 2021;597:126–131. doi: 10.1038/s41586-021-03794-8. PubMed DOI PMC
Zhao J., Chen A.Q., Ryu J., del Mármol J. Structural Basis of Odor Sensing by Insect Heteromeric Odorant Receptors. Science. 2024;384:1460–1467. doi: 10.1126/science.adn6384. PubMed DOI PMC
Wang Y., Qiu L., Wang B., Guan Z., Dong Z., Zhang J., Cao S., Yang L., Wang B., Gong Z., et al. Structural Basis for Odorant Recognition of the Insect Odorant Receptor OR-Orco Heterocomplex. Science. 2024;384:1453–1460. doi: 10.1126/science.adn6881. PubMed DOI
Zhou X., Rokas A., Berger S.L., Liebig J., Ray A., Zwiebel L.J. Chemoreceptor Evolution in Hymenoptera and Its Implications for the Evolution of Eusociality. Genome Biol. Evol. 2015;7:2407–2416. doi: 10.1093/gbe/evv149. PubMed DOI PMC
Yuvaraj J.K., Roberts R.E., Sonntag Y., Hou X.Q., Grosse-Wilde E., Machara A., Zhang D.D., Hansson B.S., Johanson U., Löfstedt C., et al. Putative Ligand Binding Sites of Two Functionally Characterized Bark Beetle Odorant Receptors. BMC Biol. 2021;19:16. doi: 10.1186/s12915-020-00946-6. PubMed DOI PMC
Croset V., Rytz R., Cummins S.F., Budd A., Brawand D., Kaessmann H., Gibson T.J., Benton R. Ancient Protostome Origin of Chemosensory Ionotropic Glutamate Receptors and the Evolution of Insect Taste and Olfaction. PLoS Genet. 2010;6:e1001064. doi: 10.1371/journal.pgen.1001064. PubMed DOI PMC
Clyne P.J., Warr C.G., Carlson J.R. Candidate Taste Receptors in Drosophila. Science. 2000;287:1830–1834. doi: 10.1126/science.287.5459.1830. PubMed DOI
Scott K., Brady R., Cravchik A., Morozov P., Rzhetsky A., Zuker C., Axel R., Brady R., Jr., Cravchik A., Morozov P., et al. A Chemosensory Gene Family Encoding Candidate Gustatory and Olfactory Receptors in Drosophila. Cell. 2001;104:661–673. doi: 10.1016/S0092-8674(01)00263-X. PubMed DOI
Weiss L.A., Dahanukar A., Kwon J.Y., Banerjee D., Carlson J.R. The Molecular and Cellular Basis of Bitter Taste in Drosophila. Neuron. 2011;69:258–272. doi: 10.1016/j.neuron.2011.01.001. PubMed DOI PMC
Montell C. A Taste of the Drosophila Gustatory Receptors. Curr. Opin. Neurobiol. 2009;19:345–353. doi: 10.1016/j.conb.2009.07.001. PubMed DOI PMC
Leal W.S. Odorant Reception in Insects: Roles of Receptors, Binding Proteins, and Degrading Enzymes. Annu. Rev. Entomol. 2013;58:373–391. doi: 10.1146/annurev-ento-120811-153635. PubMed DOI
Gomez-Diaz C., Bargeton B., Abuin L., Bukar N., Reina J.H., Bartoi T., Graf M., Ong H., Ulbrich M.H., Masson J.F., et al. A CD36 Ectodomain Mediates Insect Pheromone Detection via a Putative Tunnelling Mechanism. Nat. Commun. 2016;7:11866. doi: 10.1038/ncomms11866. PubMed DOI PMC
Lautenschlager C., Leal W.S., Clardy J. Bombyx mori Pheromone-Binding Protein Binding Non-Pheromone Ligands: Implications for Pheromone Recognition. Structure. 2007;15:1148–1154. doi: 10.1016/j.str.2007.07.013. PubMed DOI PMC
Pelosi P., Iovinella I., Felicioli A., Dani F.R., Kadarkarai M.E. Soluble Proteins of Chemical Communication: An Overview across Arthropods. Front. Physiol. 2014;5:320. doi: 10.3389/fphys.2014.00320. PubMed DOI PMC
Venthur H., Mutis A., Zhou J.J., Quiroz A. Ligand Binding and Homology Modelling of Insect Odorant-Binding Proteins. Physiol. Entomol. 2014;39:183–198. doi: 10.1111/phen.12066. DOI
Pelosi P., Iovinella I., Zhu J., Wang G., Dani F.R. Beyond Chemoreception: Diverse Tasks of Soluble Olfactory Proteins in Insects. Biol. Rev. 2018;93:184–200. doi: 10.1111/brv.12339. PubMed DOI
Vogt R.G., Miller N.E., Litvack R., Fandino R.A., Sparks J., Staples J., Friedman R., Dickens J.C. The Insect SNMP Gene Family. Insect Biochem. Mol. Biol. 2009;39:448–456. doi: 10.1016/j.ibmb.2009.03.007. PubMed DOI
Rogers M.E., Sun M., Lerner M.R., Vogt R.G. Snmp-1, a Novel Membrane Protein of Olfactory Neurons of the Silk Moth Antheraea polyphemus with Homology to the CD36 Family of Membrane Proteins. J. Biol. Chem. 1997;272:14792–14799. doi: 10.1074/jbc.272.23.14792. PubMed DOI
Cassau S., Krieger J. Evidence for a Role of SNMP2 and Antennal Support Cells in Sensillum Lymph Clearance Processes of Moth Pheromone-Responsive Sensilla. Insect Biochem. Mol. Biol. 2024;164:104046. doi: 10.1016/j.ibmb.2023.104046. PubMed DOI
Cassau S., Sander D., Karcher T., Laue M., Hause G., Breer H., Krieger J. The Sensilla-Specific Expression and Subcellular Localization of SNMP1 and SNMP2 Reveal Novel Insights into Their Roles in the Antenna of the Desert Locust Schistocerca gregaria. Insects. 2022;13:579. doi: 10.3390/insects13070579. PubMed DOI PMC
Johny J., Nihad M., Alharbi H.A., AlSaleh M.A., Antony B. Silencing Sensory Neuron Membrane Protein RferSNMPu1 Impairs Pheromone Detection in the Invasive Asian Palm Weevil. Sci. Rep. 2024;14:16541. doi: 10.1038/s41598-024-67309-x. PubMed DOI PMC
Gonzalez F., Johny J., Walker W.B., Guan Q., Mfarrej S., Jakše J., Montagné N., Jacquin-Joly E., Alqarni A.A., Al-Saleh M.A., et al. Antennal Transcriptome Sequencing and Identification of Candidate Chemoreceptor Proteins from an Invasive Pest, the American Palm Weevil, Rhynchophorus palmarum. Sci. Rep. 2021;11:8334. doi: 10.1038/s41598-021-87348-y. PubMed DOI PMC
Antony B., Johny J., Montagné N., Jacquin-Joly E., Capoduro R., Cali K., Persaud K., Al-Saleh M.A., Pain A. Pheromone Receptor of the Globally Invasive Quarantine Pest of the Palm Tree, the Red Palm Weevil (Rhynchophorus ferrugineus) Mol. Ecol. 2021;30:2025–2039. doi: 10.1111/mec.15874. PubMed DOI
Powell D., Groβe-Wilde E., Krokene P., Roy A., Chakraborty A., Löfstedt C., Vogel H., Andersson M.N., Schlyter F. A Highly-Contiguous Genome Assembly of the Eurasian Spruce Bark Beetle, Ips typographus, Provides Insight into a Major Forest Pest. Commun. Biol. 2021;4:1059. doi: 10.1038/s42003-021-02602-3. PubMed DOI PMC
Roberts R.E., Biswas T., Yuvaraj J.K., Grosse-Wilde E., Powell D., Hansson B.S., Löfstedt C., Andersson M.N. Odorant Receptor Orthologues in Conifer-Feeding Beetles Display Conserved Responses to Ecologically Relevant Odours. Mol. Ecol. 2022;31:3693–3707. doi: 10.1111/mec.16494. PubMed DOI PMC
Hou X.-Q., Yuvaraj J.K., Roberts R.E., Zhang D.-D., Unelius C.R., Löfstedt C., Andersson M.N. Functional Evolution of a Bark Beetle Odorant Receptor Clade Detecting Monoterpenoids of Different Ecological Origins. Mol. Biol. Evol. 2021;38:4934–4947. doi: 10.1093/molbev/msab218. PubMed DOI PMC
Andersson M.N., Grosse-Wilde E., Keeling C.I., Bengtsson J.M., Yuen M.M.S.S., Li M., Hillbur Y., Bohlmann J., Hansson B.S., Schlyter F. Antennal Transcriptome Analysis of the Chemosensory Gene Families in the Tree Killing Bark Beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae) BMC Genom. 2013;14:198. doi: 10.1186/1471-2164-14-198. PubMed DOI PMC
Kim D., Paggi J.M., Park C., Bennett C., Salzberg S.L. Graph-Based Genome Alignment and Genotyping with HISAT2 and HISAT-Genotype. Nat. Biotechnol. 2019;37:907–915. doi: 10.1038/s41587-019-0201-4. PubMed DOI PMC
Simão F.A., Waterhouse R.M., Ioannidis P., Kriventseva E.V., Zdobnov E.M. BUSCO: Assessing Genome Assembly and Annotation Completeness with Single-Copy Orthologs. Bioinformatics. 2015;31:3210–3212. doi: 10.1093/bioinformatics/btv351. PubMed DOI
Mitchell R.F., Schneider T.M., Schwartz A.M., Andersson M.N., McKenna D.D. The Diversity and Evolution of Odorant Receptors in Beetles (Coleoptera) Insect Mol. Biol. 2020;29:77–91. doi: 10.1111/imb.12611. PubMed DOI
Mitchell R.F., Hughes D.T., Luetje C.W., Millar J.G., Soriano-Agaton F., Hanks L.M., Robertson H.M. Sequencing and Characterizing Odorant Receptors of the Cerambycid Beetle Megacyllene caryae. Insect Biochem. Mol. Biol. 2012;42:499–505. doi: 10.1016/j.ibmb.2012.03.007. PubMed DOI PMC
Andersson M.N., Keeling C.I., Mitchell R.F. Genomic Content of Chemosensory Genes Correlates with Host Range in Wood-Boring Beetles (Dendroctonus ponderosae, Agrilus planipennis, and Anoplophora glabripennis) BMC Genom. 2019;20:690. doi: 10.1186/s12864-019-6054-x. PubMed DOI PMC
Joseph R.M., Carlson J.R. Drosophila Chemoreceptors: A Molecular Interface Between the Chemical World and the Brain. Trends Genet. 2015;31:683–695. doi: 10.1016/j.tig.2015.09.005. PubMed DOI PMC
Delventhal R., Carlson J.R. Bitter Taste Receptors Confer Diverse Functions to Neurons. Elife. 2016;5:e11181. doi: 10.7554/eLife.11181. PubMed DOI PMC
Chahda J.S., Soni N., Sun J.S., Ebrahim S.A.M., Weiss B.L., Carlson J.R. The Molecular and Cellular Basis of Olfactory Response to Tsetse Fly Attractants. PLoS Genet. 2019;15:e1008005. doi: 10.1371/journal.pgen.1008005. PubMed DOI PMC
Dahanukar A., Foster K., van der Goes van Naters W.M., Carlson J.R. A Gr Receptor Is Required for Response to the Sugar Trehalose in Taste Neurons of Drosophila. Nat. Neurosci. 2001;4:1182–1186. doi: 10.1038/nn765. PubMed DOI
Bray S., Amrein H. A Putative Drosophila Pheromone Receptor Expressed in Male-Specific Taste Neurons Is Required for Efficient Courtship. Neuron. 2003;39:1019–1029. doi: 10.1016/S0896-6273(03)00542-7. PubMed DOI
Andrews J.C., Fernández M.P., Yu Q., Leary G.P., Leung A.K.W., Kavanaugh M.P., Kravitz E.A., Certel S.J. Octopamine Neuromodulation Regulates Gr32a-Linked Aggression and Courtship Pathways in Drosophila Males. PLoS Genet. 2014;10:e1004356. doi: 10.1371/journal.pgen.1004356. PubMed DOI PMC
Hekmat-Scafe D.S., Scafe C.R., McKinney A.J., Tanouye M.A. Genome-Wide Analysis of the Odorant-Binding Protein Gene Family in Drosophila melanogaster. Genome Res. 2002;12:1357–1369. doi: 10.1101/gr.239402. PubMed DOI PMC
Sánchez-Gracia A., Rozas J. Divergent Evolution and Molecular Adaptation in the Drosophila Odorant-Binding Protein Family: Inferences from Sequence Variation at the OS-E and OS-F Genes. BMC Evol. Biol. 2008;8:323. doi: 10.1186/1471-2148-8-323. PubMed DOI PMC
Venthur H., Zhou J.-J. Odorant Receptors and Odorant-Binding Proteins as Insect Pest Control Targets: A Comparative Analysis. Front. Physiol. 2018;9:1163. doi: 10.3389/fphys.2018.01163. PubMed DOI PMC
Große-Wilde E., Svatoš A., Krieger J. A Pheromone-Binding Protein Mediates the Bombykol-Induced Activation of a Pheromone Receptor in vitro. Chem. Senses. 2006;31:547–555. doi: 10.1093/chemse/bjj059. PubMed DOI
Antony B., Johny J., Aldosari S.A. Silencing the Odorant Binding Protein RferOBP1768 Reduces the Strong Preference of Palm Weevil for the Major Aggregation Pheromone Compound Ferrugineol. Front. Physiol. 2018;9:252. doi: 10.3389/fphys.2018.00252. PubMed DOI PMC
Wojtasek H., Hansson B.S., Leal W.S. Attracted or Repelled?—A Matter of Two Neurons, One Pheromone Binding Protein, and a Chiral Center. Biochem. Biophys. Res. Commun. 1998;250:217–222. doi: 10.1006/bbrc.1998.9278. PubMed DOI
Pelosi P., Zhou J., Ban L.P., Calvello M. Soluble Proteins in Insect Chemical Communication. Cell. Mol. Life Sci. 2006;63:1658–1676. doi: 10.1007/s00018-005-5607-0. PubMed DOI PMC
Schiebe C., Blaženec M., Jakuš R., Unelius C.R., Schlyter F. Semiochemical Diversity Diverts Bark Beetle Attacks from Norway Spruce Edges. J. Appl. Entomol. 2011;135:726–737. doi: 10.1111/j.1439-0418.2011.01624.x. DOI
Antony B., Soffan A., Jakše J., Abdelazim M.M., Aldosari S.A., Aldawood A.S., Pain A. Identification of the Genes Involved in Odorant Reception and Detection in the Palm Weevil Rhynchophorus ferrugineus, an Important Quarantine Pest, by Antennal Transcriptome Analysis. BMC Genom. 2016;17:69. doi: 10.1186/s12864-016-2362-6. PubMed DOI PMC
Johny J., Diallo S., Lukšan O., Shewale M., Kalinová B., Hanus R., Große-Wilde E. Conserved Orthology in Termite Chemosensory Gene Families. Front. Ecol. Evol. 2023;10:1065947. doi: 10.3389/fevo.2022.1065947. DOI
Yuvaraj J.K., Roberts R.E., Hansson B.S., Andersson M.N. Eurasian Spruce Bark Beetle Detects Anti-Attractant Lanierone Using a Highly Expressed Specialist Odorant Receptor, Present in Several Functional Sensillum Types. Res. Sq. 2024 doi: 10.21203/rs.3.rs-3681257/v2. in press . DOI
Wang X., Wang S., Yi J., Li Y., Liu J., Wang J., Xi J. Three Host Plant Volatiles, Hexanal, Lauric Acid, and Tetradecane, Are Detected by an Antenna-Biased Expressed Odorant Receptor 27 in the Dark Black Chafer Holotrichia parallela. J. Agric. Food Chem. 2020;68:7316–7323. doi: 10.1021/acs.jafc.0c00333. PubMed DOI
Antony B., Montagné N., Comte A., Mfarrej S., Jakše J., Capoduro R., Shelke R., Cali K., AlSaleh M.A., Persaud K., et al. Deorphanizing an Odorant Receptor Tuned to Palm Tree Volatile Esters in the Asian Palm Weevil Sheds Light on the Mechanisms of Palm Tree Selection. Insect Biochem. Mol. Biol. 2024;169:104129. doi: 10.1016/j.ibmb.2024.104129. PubMed DOI
Ji T., Xu Z., Jia Q., Wang G., Hou Y. Non-Palm Plant Volatile α-Pinene Is Detected by Antenna-Biased Expressed Odorant Receptor 6 in the Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae) Front. Physiol. 2021;12:701545. doi: 10.3389/fphys.2021.701545. PubMed DOI PMC
Brajon L., Comte A., Capoduro R., Meslin C., Antony B., Al-Saleh M.A., Pain A., Jacquin-Joly E., Montagné N. A Conserved Pheromone Receptor in the American and the Asian Palm Weevils Is Also Activated by Host Plant Volatiles. Curr. Res. Insect Sci. 2024;6:100090. doi: 10.1016/j.cris.2024.100090. PubMed DOI PMC
Anderson A.R., Newcomb R.D. Olfactory Genomics and Biotechnology in Insect Control. In: Blomquist G.J., Vogt R.G., editors. Insect Pheromone Biochemistry and Molecular Biology. 2nd ed. Elsevier; London, UK: 2021. pp. 645–674.
Bohbot J.D., Vernick S. The Emergence of Insect Odorant Receptor-Based Biosensors. Biosensors. 2020;10:26. doi: 10.3390/bios10030026. PubMed DOI PMC
Hoddle M., Antony B., El-Shafie H., Chamorro L., Milosavljević I., Bernhard L., Faleiro R. Taxonomy, Biology, Symbionts, Omics, and Management of Rhynchophorus Palm Weevils (Coleoptera: Curculionidae: Dryophthorinae) Annu. Rev. Entomol. 2024;69:449–479. doi: 10.1146/annurev-ento-013023-121139. PubMed DOI
Arntsen C., Guillemin J., Audette K., Stanley M. Tastant-Receptor Interactions: Insights from the Fruit Fly. Front. Nutr. 2024;11:3–5. doi: 10.3389/fnut.2024.1394697. PubMed DOI PMC
Liu N.-Y., Li Z.-B., Zhao N., Song Q.-S., Zhu J.-Y., Yang B. Identification and Characterization of Chemosensory Gene Families in the Bark Beetle, Tomicus yunnanensis. Comp. Biochem. Physiol. Part D Genom. Proteom. 2018;25:73–85. doi: 10.1016/j.cbd.2017.11.003. PubMed DOI
Zhou J.J., Huang W., Zhang G.A., Pickett J.A., Field L.M. “Plus-C” Odorant-Binding Protein Genes in Two Drosophila Species and the Malaria Mosquito Anopheles gambiae. Gene. 2004;327:117–129. doi: 10.1016/j.gene.2003.11.007. PubMed DOI
Rihani K., Ferveur J.F., Briand L. The 40-Year Mystery of Insect Odorant-Binding Proteins. Biomolecules. 2021;11:509. doi: 10.3390/biom11040509. PubMed DOI PMC
Pelosi P., Zhu J., Knoll W. Odorant-Binding Proteins as Sensing Elements for Odour Monitoring. Sensors. 2018;18:3248. doi: 10.3390/s18103248. PubMed DOI PMC
Tegoni M., Campanacci V., Cambillau C. Structural Aspects of Sexual Attraction and Chemical Communication in Insects. Trends Biochem. Sci. 2004;29:257–264. doi: 10.1016/j.tibs.2004.03.003. PubMed DOI
Vogt R.G. Biochemical Diversity of Odor Detection. In: Blomquist G., Vogt R., editors. Insect Pheromone Biochemistry and Molecular Biology. Elsevier; San Diego, CA, USA: 2003. pp. 391–445.
German P.F., van der Poel S., Carraher C., Kralicek A.V., Newcomb R.D. Insights into Subunit Interactions within the Insect Olfactory Receptor Complex Using FRET. Insect Biochem. Mol. Biol. 2013;43:138–145. doi: 10.1016/j.ibmb.2012.11.002. PubMed DOI
Nichols Z., Vogt R.G. The SNMP/CD36 Gene Family in Diptera, Hymenoptera and Coleoptera: Drosophila melanogaster, D. pseudoobscura, Anopheles gambiae, Aedes aegypti, Apis mellifera, and Tribolium castaneum. Insect Biochem. Mol. Biol. 2008;38:398–415. doi: 10.1016/j.ibmb.2007.11.003. PubMed DOI
Rogers M.E., Steinbrecht R.A., Vogt R.G. Expression of SNMP-1 in Olfactory Neurons and Sensilla of Male and Female Antennae of the Silkmoth Antheraea polyphemus. Cell Tissue Res. 2001;303:433–446. doi: 10.1007/s004410000305. PubMed DOI
Ewels P., Magnusson M., Lundin S., Käller M. MultiQC: Summarise Analysis Results for Multiple Tools and Samples in a Single Report. Bioinformatics. 2016;32:3047–3048. doi: 10.1093/bioinformatics/btw354. PubMed DOI PMC
Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q., et al. Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome. Nat. Biotechnol. 2011;29:644–652. doi: 10.1038/nbt.1883. PubMed DOI PMC
Fu L., Niu B., Zhu Z., Wu S., Li W. CD-HIT: Accelerated for Clustering the next-Generation Sequencing Data. Bioinformatics. 2012;28:3150–3152. doi: 10.1093/bioinformatics/bts565. PubMed DOI PMC
Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T.L. BLAST+: Architecture and Applications. BMC Bioinform. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC
Dippel S., Kollmann M., Oberhofer G., Montino A., Knoll C., Krala M., Rexer K., Frank S., Kumpf R., Schachtner J., et al. Morphological and Transcriptomic Analysis of a Beetle Chemosensory System Reveals a Gnathal Olfactory Center. BMC Biol. 2016;14:90. doi: 10.1186/s12915-016-0304-z. PubMed DOI PMC
Liu Y., Sun L., Cao D., Walker W.B., Zhang Y., Wang G. Identification of Candidate Olfactory Genes in Leptinotarsa decemlineata by Antennal Transcriptome Analysis. Front. Ecol. Evol. 2015;3:60. doi: 10.3389/fevo.2015.00060. DOI
Frickey T., Lupas A. CLANS: A Java Application for Visualizing Protein Families Based on Pairwise Similarity. Bioinformatics. 2004;20:3702–3704. doi: 10.1093/bioinformatics/bth444. PubMed DOI
Hallgren J., Tsirigos K.D., Damgaard Pedersen M., Juan J., Armenteros A., Marcatili P., Nielsen H., Krogh A., Winther O. DeepTMHMM Predicts Alpha and Beta Transmembrane Proteins Using Deep Neural Networks. bioRxiv. 2022 bioRxiv:2022.04.08.487609.
Tsirigos K.D., Peters C., Shu N., Käll L., Elofsson A. The TOPCONS Web Server for Consensus Prediction of Membrane Protein Topology and Signal Peptides. Nucleic Acids Res. 2015;43:W401–W407. doi: 10.1093/nar/gkv485. PubMed DOI PMC
Vogt R.G., Große-Wilde E., Zhou J.J. The Lepidoptera Odorant Binding Protein Gene Family: Gene Gain and Loss within the GOBP/PBP Complex of Moths and Butterflies. Insect Biochem. Mol. Biol. 2015;62:142–153. doi: 10.1016/j.ibmb.2015.03.003. PubMed DOI
Guo W., Ren D., Zhao L., Jiang F., Song J., Wang X., Kang L. Identification of Odorant-Binding Proteins (OBPs) and Functional Analysis of Phase-Related OBPs in the Migratory Locust. Front. Physiol. 2018;9:984. doi: 10.3389/fphys.2018.00984. PubMed DOI PMC
Felsenstein J. Evolutionary Trees from DNA Sequences: A Maximum Likelihood Approach. J. Mol. Evol. 1981;17:368–376. doi: 10.1007/BF01734359. PubMed DOI
Saina M., Busengdal H., Sinigaglia C., Petrone L., Oliveri P., Rentzsch F., Benton R. A Cnidarian Homologue of an Insect Gustatory Receptor Functions in Developmental Body Patterning. Nat. Commun. 2015;6:6243. doi: 10.1038/ncomms7243. PubMed DOI PMC
Maïbèche-Coisne M., Nikonov A.A., Ishida Y., Jacquin-Joly E., Leal W.S. Pheromone Anosmia in a Scarab Beetle Induced by in vivo Inhibition of a Pheromone-Degrading Enzyme. Proc. Natl. Acad. Sci. USA. 2004;101:11459–11464. doi: 10.1073/pnas.0403537101. PubMed DOI PMC
Missbach C., Vogel H., Hansson B.S., Große-Wilde E. Identification of Odorant Binding Proteins and Chemosensory Proteins in Antennal Transcriptomes of the Jumping Bristletail Lepismachilis y-signata and the Firebrat Thermobia domestica: Evidence for an Independent OBP-OR Origin. Chem. Senses. 2015;40:615–626. doi: 10.1093/chemse/bjv050. PubMed DOI
Zhou J.-J., Robertson G., He X., Dufour S., Hooper A.M., Pickett J.A., Keep N.H., Field L.M. Characterisation of Bombyx mori Odorant-Binding Proteins Reveals That a General Odorant-Binding Protein Discriminates Between Sex Pheromone Components. J. Mol. Biol. 2009;389:529–545. doi: 10.1016/j.jmb.2009.04.015. PubMed DOI
Zhao Y.J., Li G.C., Zhu J.Y., Liu N.Y. Genome-Based Analysis Reveals a Novel SNMP Group of the Coleoptera and Chemosensory Receptors in Rhaphuma horsfieldi. Genomics. 2020;112:2713–2728. doi: 10.1016/j.ygeno.2020.03.005. PubMed DOI
Katoh K., Rozewicki J., Yamada K.D. MAFFT Online Service: Multiple Sequence Alignment, Interactive Sequence Choice and Visualization. Brief. Bioinform. 2017;20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC
Capella-Gutiérrez S., Silla-Martínez J.M., Gabaldón T. TrimAl: A Tool for Automated Alignment Trimming in Large-Scale Phylogenetic Analyses. Bioinformatics. 2009;25:1972–1973. doi: 10.1093/bioinformatics/btp348. PubMed DOI PMC
Darriba D., Taboada G.L., Doallo R., Posada D. ProtTest 3: Fast Selection of Best-Fit Models of Protein Evolution. Bioinformatics. 2017;27:1164–1165. doi: 10.1093/bioinformatics/btr088. PubMed DOI PMC
Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., Von Haeseler A., Lanfear R., Teeling E. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC
Shimodaira H., Hasegawa M. Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference. Mol. Biol. Evol. 1999;16:1114–1116. doi: 10.1093/oxfordjournals.molbev.a026201. DOI
Teufel F., Almagro Armenteros J.J., Johansen A.R., Gíslason M.H., Pihl S.I., Tsirigos K.D., Winther O., Brunak S., von Heijne G., Nielsen H. SignalP 6.0 Predicts All Five Types of Signal Peptides Using Protein Language Models. Nat. Biotechnol. 2022;40:1023–1025. doi: 10.1038/s41587-021-01156-3. PubMed DOI PMC
Wang J., Chitsaz F., Derbyshire M.K., Gonzales N.R., Gwadz M., Lu S., Marchler G.H., Song J.S., Thanki N., Yamashita R.A., et al. The Conserved Domain Database in 2023. Nucleic Acids Res. 2023;51:D384–D388. doi: 10.1093/nar/gkac1096. PubMed DOI PMC
Abramson J., Adler J., Dunger J., Evans R., Green T., Pritzel A., Ronneberger O., Willmore L., Ballard A.J., Bambrick J., et al. Accurate Structure Prediction of Biomolecular Interactions with AlphaFold 3. Nature. 2024;630:493–500. doi: 10.1038/s41586-024-07487-w. PubMed DOI PMC
Meng E.C., Goddard T.D., Pettersen E.F., Couch G.S., Pearson Z.J., Morris J.H., Ferrin T.E. UCSF ChimeraX: Tools for Structure Building and Analysis. Protein Sci. 2023;32:e4792. doi: 10.1002/pro.4792. PubMed DOI PMC