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Identification of candidate chemosensory receptors in the antennal transcriptome of Tropidothorax elegans

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Abstract

Chemosensory receptors in the dendritic membrane of olfactory cells are critical for the molecular recognition and discrimination of odorants. Tropidothorax elegans is a major pest of agricultural, ornamental, and medicinal plants. However, very little is known about olfactory genes in T. elegans. The purpose of this study was to obtain chemosensory receptor genes by sequencing the antennal transcriptome of T. elegans using Illumina sequencing technology. We identified 153 candidate chemosensory receptors, including 121 olfactory receptors (including one olfactory receptor co-receptor), 10 ionotropic receptors (including one IR8a and one IR25a), and 22 gustatory receptors (GRs). TeleOR76, 104 and 112 displayed more highly expression level than TeleOrco. Other TeleGR genes were expressed at very low levels except TeleGR1 and 20. TeleIR76b was the most highly expressed among TeleIR genes. Our results provide valuable biological information for studies of the olfactory communication system of T. elegans.

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References

  1. Kaupp UB (2010) Olfactory signalling in vertebrates and insects: differences and commonalities. Nat Rev Neurosci 11:188–200

    Article  CAS  PubMed  Google Scholar 

  2. Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391

    Article  CAS  PubMed  Google Scholar 

  3. Maida R, Proebstl T, Laue M (1997) Heterogeneity of odorant-binding proteins in the antennae of Bombyx mori. Chem Sens 22:503–515

    Article  CAS  Google Scholar 

  4. Klein U (1987) Sensillum-lymph proteins from antennal olfactory hairs of the moth Antheraea polyphemus (Saturniidae). Insect Biochem Mol 17:1193–1204

    Article  Google Scholar 

  5. Jacquin-Joly E, Vogt RG, François MC, Nagnan-Le Meillour P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chem Sens 26:833–844

    Article  CAS  Google Scholar 

  6. Leal WS (2012) Odorant reception in insects: roles of receptors, binding proteins and degrading enzymes. Annu Rev Entomol 58:373–391

    Article  PubMed  Google Scholar 

  7. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187

    Article  CAS  PubMed  Google Scholar 

  8. Benton R, Vannice KS, Vosshall LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450:289–293

    Article  CAS  PubMed  Google Scholar 

  9. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    Article  CAS  PubMed  Google Scholar 

  10. Sato K, Pellegrino M, Nakagawa T, Nakagawa T, Vosshall LB, Touhara K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452:1002–1006

    Article  CAS  PubMed  Google Scholar 

  11. Wicher D, Schfer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclicnucleotide-activated cation channels. Nature 452:1007–1011

    Article  CAS  PubMed  Google Scholar 

  12. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, Chrystal MA, Cravchik A, Collins FH, Robertson HM, Zwiebel LJ (2002) G protein-coupled receptors in Anopheles gambiae. Science 298:176–178

    Article  CAS  PubMed  Google Scholar 

  13. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci 100:14537–14542

    Article  CAS  PubMed  Google Scholar 

  14. Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory receptor family. Genome Res 16:1395–1403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wanner KW, Robertson HM (2008) The gustatory receptor family in the silkworm moth Bombyx mori is characterized by a large expansion of a single lineage of putative bitter receptors. Insect Mol Biol 9:621–629

    Article  Google Scholar 

  16. Dahanukar A, Lei YT, Kwon JY, Carlson JR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56:503–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822–835

    Article  CAS  PubMed  Google Scholar 

  18. Hiroi M, Marion-Poll F, Tanimura T (2002) Differentiated response to sugars among labellar chemosensilla in Drosophila. Zool Sci 19:1009–1018

    Article  Google Scholar 

  19. Jones WD, Cayirlioglu P, Grunwald Kadow I, Vosshall LB (2007) Two chemosensory receptors together mediatecarbon dioxide detection in Drosophila. Nature 445:86–90

    Article  CAS  PubMed  Google Scholar 

  20. Kwon JY, Dahanukar A, Weiss LA, Carlson JR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA 104:3574–3578

    Article  CAS  PubMed  Google Scholar 

  21. Sato K, Tanaka K, Touhara K (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. PNAS 108:11680–11685

    Article  CAS  PubMed  Google Scholar 

  22. Rimal S, Lee Y (2018) The multidimensional ionotropic receptors of Drosophila melanogaster. Insect Mol Biol 27:1–7

    Article  CAS  PubMed  Google Scholar 

  23. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69:44–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rytz R, Croset V, Benton R (2013) Ionotropic Receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol 43:888–897

    Article  CAS  PubMed  Google Scholar 

  26. Koh TW, He Z, Gorur-Shandilya S, Menuz K, Larter NK, Stewart S, Carlson JR (2014) The Drosophila IR20a clade of ionotropic receptors are candidate taste and pheromone receptors. Neuron 83:850–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hussain A, Zhang M, Ucpunar HK, Svensson T, Quillery E, Gompel N, Ignell R, Kadow ICG (2016) Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLoS Biol 14:e1002454

    Article  PubMed  PubMed Central  Google Scholar 

  28. Li XY, Zhao XQ, Yin YQ, Chen AD, Bu WJ, Jiao KL, Li N, Hu Q (2015) Recognition of the nymph instars of eight common harmful stinkbug species in the fields. Plant Protect China 41:100–105

    Google Scholar 

  29. Song YQ, Sun HZ, Du J (2018) Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans Distant (Hemiptera: Lygaeidae). Sci Rep-UK 8:7803

    Article  Google Scholar 

  30. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Amit DA, Adiconis X et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 7:138–148

    Google Scholar 

  32. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  Google Scholar 

  33. Xu P, Choo YM, DeLa RA, Leal WS (2014) Mosquito odorant receptor for DEET and methyl jasmonate. Proc Natl Acad Sci USA 111:16592–16597

    Article  CAS  PubMed  Google Scholar 

  34. Wang R, Zhang XM, Li HL, Guo XJ, Luo C (2016) Identification and expression profiling of five chemosensory protein genes in the whitefly MED, Bemisia tabaci. J Asia Pac Entomol 19:195–201

    Article  CAS  Google Scholar 

  35. Xiao W, Yang L, Xu Z, He L (2016) Transcriptomics and identification of candidate chemosensory genes in antennae of Conogethes punctiferalis (Lepidoptera: Crambidae). J Asia Pac Entomol 19:911–920

    Article  Google Scholar 

  36. Zhang YN, Ma JM, Sun L, Dong ZP, Li ZQ, Zhu XY, Wang Y, Wang L, Deng DG, Li JB (2016) Molecular identification and sex distribution of two chemosensory receptor families in Athetis lepigone by antennal transcriptome analysis. J Asia Pac Entomol 19:571–580

    Article  Google Scholar 

  37. Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM et al (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci USA 107:12168–12173

    Article  CAS  PubMed  Google Scholar 

  38. Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M et al (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci USA 108:5667–5672

    Article  CAS  PubMed  Google Scholar 

  39. Zhang YN, Zhu XY, Zhang Q, Yin CY, Dong ZP, Zuo LH, Deng DG, Sun L, Li XM (2016) De novo assembly and characterization of antennal transcriptome reveal chemosensory system in Nysius ericae. J Asia-Pac Entomol 19:1077–1087

    Article  Google Scholar 

  40. An XK, Sun L, Liu HW, Liu DF, Ding YX, Li LM, Zhang YJ, Guo YY (2016) Identification and expression analysis of an olfactory receptor gene family in green plant bug Apolygus lucorum (Meyer-Dür). Sci Rep-UK 6:37870

    Article  CAS  Google Scholar 

  41. Xiao Y, Sun L, Ma XY, Dong K, Liu HW, Wang Q, Guo YY, Liu ZW, Zhang YJ (2017) Identification and characterization of the distinct expression profiles of candidate chemosensory membrane proteins in the antennal transcriptome of Adelphocoris lineolatus (Goeze). Insect Mol Biol 26:74–91

    Article  CAS  PubMed  Google Scholar 

  42. Engsontia P, Sanderson AP, Cobb M, Walden KK, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38:387–397

    Article  CAS  PubMed  Google Scholar 

  43. Wang Z, Yang P, Chen D, Jiang F, Li Y, Wang X, Kang L (2015) Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. Cell Mol Life Sci 72:4429–4443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. He M, Zhang YN, He P (2015) Molecular characterization and differential expression of an olfactory receptor gene family in the white-backed planthopper Sogatella furcifera based on transcriptome analysis. PLoS ONE 10:e0140605

    Article  PubMed  PubMed Central  Google Scholar 

  45. Cao D, Liu Y, Walker WB, Li J, Wang G (2014) Molecular characterization of the Aphis gossypii olfactory receptor gene families. PLoS ONE 9:e101187

    Article  PubMed  PubMed Central  Google Scholar 

  46. Sanchez-Gracia A, Vieira FG, Rozas J (2009) Molecular evolution of the major chemosensory gene families in insects. Heredity 103:208–216

    Article  CAS  PubMed  Google Scholar 

  47. Smart R, Kiely A, Beale M, Vargas E, Carraher C, Kralicek AV, Christie DL, Chen C, Newcomb RD, Warr CG (2008) Drosophila odorant receptors are novel seven transmembrane domain proteins that can signal independently of heterotrimeric G proteins. Insect Biochem Mol 38:770–780

    Article  CAS  Google Scholar 

  48. Dong JF, Song YQ, Li WL, Shi J, Wang ZY (2016) Identification of putative chemosensory receptor genes from the Athetis dissimilis antennal transcriptome. PLoS ONE 11:e0147768

    Article  PubMed  PubMed Central  Google Scholar 

  49. Andersson MN, Grosse-Wilde E, Keeling CI, Bengtsson JM, Yuen MM, Li M, Hillbur Y, Bohlmann J, Hansson BS, Schlyter F (2013) Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae). BMC Genomics 14:198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Jacquin-Joly E, Legeai F, Montagne N, Monsempes C, Francois MC, Poulain J, Gavory F, Walker WB, Hansson BS, Larsson MC (2012) Candidate chemosensory genes in female antennae of the noctuid moth Spodoptera littoralis. Int J Biol Sci 8:1036–1050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830–1834

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was funded by the National Natural Science Fund of China (31701788) and Science and Technology Project in Henan Province (202102110069).

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Authors and Affiliations

  1. Forestry College, Henan University of Science & Technology, Luoyang, 471000, China

    Yue Qin Song, Zhi Yu Song & Hui Zhong Sun

  2. Guangyuan Tobacco Corporation of Sichuan Province, Guangyuan, 628000, China

    Hui Zhan Gu

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Contributions

All authors contributed to research design and manuscript preparation. Conceived and designed the experiments: YQS and HZS. Performed the experiments: YQS and HZS. Analyzed the data: YQS, HZS and ZYS. Contributed reagents/materials/analysis tools: YQS, JYZ and ZYS. Wrote the paper: YQS and HZS. All authors read and approved the final manuscript.

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Correspondence to Hui Zhong Sun.

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Song, Y.Q., Gu, H.Z., Song, Z.Y. et al. Identification of candidate chemosensory receptors in the antennal transcriptome of Tropidothorax elegans. Mol Biol Rep 48, 3127–3143 (2021). https://doi.org/10.1007/s11033-021-06327-8

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