Log in

Identification and expression profiles of candidate chemoreceptor genes in the tea leafhopper, Empoasca onukii Matsuda (Hemiptera: Cicadellidae)

  • Research
  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

The olfactory system of insects regulates the processes of insect feeding, mating, and egg laying through the participation of various olfactory proteins, hence it plays a key role in insect survival and reproduction. The tea leafhopper, Empoasca onukii Matsuda, is one of the most devastating pests in Chinese tea plantations. Transcriptome sequencing experiments were conducted to detect chemoreceptor genes including odorant receptors/co-receptors (ORs/Orco), ionotropic receptors (IRs), N-methyl-D-aspartic acid receptors (NMDAs), gustatory receptors (GRs), and sensory neuron membrane proteins (SNMPs). Phylogenetic analysis of chemoreceptor genes and the expression levels of the identified genes in four different tissues of E. onukii, including antennae, heads, bodies, and legs were also analyzed. In total, 12 ORs, five IRs, three NMDAs, three GRs, and two SNMPs were annotated in the E. onukii transcriptome data. The number of chemoreceptor genes in E. onukii was considerably lower than that in other hemiptera insects. Phylogenetic analysis was conducted to compare ORs, IRs, NMDAs, GRs, and SNMPs among the hemiptera insects, and showed that chemoreceptor genes in E.onukii were clustered into ten clades with other hemiptera insects, respectively. The results of RT-qPCR showed that seven EonuORs, three EonuIRs, and one EonuGRs were highly expressed in the antennae of E. onukii. The function of chemoreceptor genes in E. onukii in sensing the volatile compounds remains to be elucidated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The transcriptome sequences were deposited in the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/guide/).

References

  • Agnihotri, A. R., Roy, A. A., & Joshi, R. S. (2016). Gustatory receptors in Lepidoptera: Chemosensation and beyond. Insect Molecular Biology, 25, 519–529.

    Article  CAS  PubMed  Google Scholar 

  • Ahashaveh, A., An, X. K., Shan, S., **ao, Y., Wang, Q., Wang, Z. B., Geng, T., Gu, S. H., & Zhang, Y. J. (2019). Deorphanization of an odorant receptor revealed new bioactive components for green mirid bug Apolygus lucorum (Hemiptera: Miridae). Pest Management Science, 76, 126–1638.

    Google Scholar 

  • An, X. K., Sun, L., Liu, H. W., Liu, D. F., Ding, Y. X., Li, L. M., & Guo, Y. Y. (2016). Identification and expression analysis of an olfactory receptor gene family in green plant bug Apolygus lucorum (Meyer-Dür). Scientific Reports, 6, 37870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bian, L., Cai, X. M., Luo, Z. X., Li, Z. Q., & Chen, Z. M. (2021). Sticky card for Empoasca onukii with bicolor patterns captures less beneficial arthropods in tea gardens. Crop Protection, 149, 105761.

    Article  Google Scholar 

  • Cai, X., Luo, Z., Meng, Z., Liu, Y., Chu, B., Bian, L., & Chen, Z. (2020). Primary screening and application of repellent plant volatiles to control tea leafhopper, Empoasca onukii Matsuda. Pest Management Science, 76, 1304–1312.

    Article  CAS  PubMed  Google Scholar 

  • Cassau, S., & Krieger, J. (2020). The role of SNMPs in insect olfaction. Cell and Tissue Research, 383, 21–33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng, J., Wang, C. Y., Lyu, Z. H., Chen, J. X., Tang, L. P., & Lin, T. (2018). Candidate olfactory genes identified in Heortia vitessoides (Lepidoptera: Crambidae) by antennal transcriptome analysis. Comparative Biochemistry and Physiology Part d: Genomics and Proteomics, 29, 117–130.

    Google Scholar 

  • Croset, V., Rytz, R., Cummins, S. F., Budd, A., Brawand, D., Kaessmann, H., & Benton, R. (2010). Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics, 6, e1001064.

    Article  PubMed  PubMed Central  Google Scholar 

  • Forstner, M., Gohl, T., Gondesen, I., Raming, K., Breer, H., & Krieger, J. (2008). Differential expression of SNMP-1 and SNMP-2 proteins in pheromone-sensitive hairs of moths. Chemial Senses, 33, 291–299.

    Article  CAS  Google Scholar 

  • Gouin, A., Bretaudeau, A., Nam, K., Gimenez, S., Aury, J. M., Duvic, B., & Fournier, P. (2017). Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. Scientific Reports, 7, 11816.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo, J. M., & Dong, S. L. (2020). Research progress in ionotropic receptors and their functions in insects. Acta Entomologica Sinica, 63, 1399–1410.

    Google Scholar 

  • He, M., Zhang, Y. N., & 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 

  • He, P., Chen, G. L., Li, S., Wang, J., Ma, Y. F., Pan, Y. F., & He, M. (2019). Evolution and functional analysis of odorant binding proteins in three rice planthoppers: Nilaparvata lugens, Sogatella furcifera, and Laodelphax striatellus. Pest Management Science, 75, 1606–1620.

    Article  CAS  PubMed  Google Scholar 

  • Hou, B. H., Tang, H., Li, J. L., Meng, X., & Ouyang, G. C. (2020). Susceptibility of Selected Tea Shoots to Oviposition by Empoasca onukii (Hemiptera: Cicadellidae) and Feasibility of Egg Removal with Harvesting. Insects, 11, 338.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang, T. Y., Zhang, R. B., Yang, L. L., Cao, S., Frederic, F., Wang, B., & Wang, G. R. (2022). Identification and functional characterization of ApisOr23 in pea aphid Acyrthosiphon pisum. Journal of Integrative Agriculture, 21, 1414–1423.

    Article  CAS  Google Scholar 

  • **, X., Ha, T. S., & Smith, D. P. (2008). SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proceedings of the National Academy of Sciences of the United of America, 105, 10996–11001.

    Article  CAS  Google Scholar 

  • Kang, Z. W., Liu, F. H., Pang, R. P., Yu, W. B., Tan, X. L., Zheng, Z. Q., & Liu, T. X. (2018). The identification and expression analysis of candidate chemosensory genes in the bird cherry-oat aphid Rhopalosiphum padi (L.). Bulletin of Entomological Research, 108, 645–657.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Ni, J. D., Huang, J., & Montell, C. (2014). Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity. PLoS Genetics, 10, e1004600.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, N. Y., Wei, X., Papanicolaou, A., Dong, S. L., & Anderson, A. (2014). Identification and characterization of three chemosensory receptor families in the cotton bollworm Helicoverpa armigera. BMC Genomics, 15, 597.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu, Z., Wang, X., Lei, C., & Zhu, F. (2017). Sensory genes identification with head transcriptome of the migratory armyworm Mythimna separata. Scientific Reports, 7, 46033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, F., Ye, Z., Baker, A., Sun, H., & Zwiebel, L. J. (2020a). Gene editing reveals obligate and modulatory components of the CO2 receptor complex in the malaria vector mosquito, Anopheles coluzzii. Insect Biochemistry and Molecular Biology, 127, 103470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., Du, L., Zhu, Y., Yang, S., Zhou, Q., Wang, G., & Liu, Y. (2020b). Identification and sex-biased profiles of candidate olfactory genes in the antennal transcriptome of the parasitoid wasp Cotesia vestalis. Comparative Biochemistry and Physiology Part d: Genomics and Proteomics, 34, 100657.

    CAS  Google Scholar 

  • Liu, Z. H., Chen, Z. M., Yang, Y. J., & Jiang, R. H. (2021). Innovation Drives High-quality Development of Chinese Tea Industry—from Basic Research of Tea Science to Supporting Industrial Development. China Tea, 43, 1–9.

    CAS  Google Scholar 

  • Nakagawa, T., Pellegrino, M., Sato, K., Vosshall, L. B., & Touhara, K. (2012). Amino Acid Residues Contributing to Function of the Heteromeric Insect Olfactory Receptor Complex. PLoS One, 7, e32372. https://doi.org/10.1371/journal.pone.0032372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olivier, V., Monsempes, C., Francois, M. C., Poivet, E., & Jacquin-Joly, E. (2011). Candidate chemosensory ionotropic receptors in a Lepidoptera. Insect Molecular Biology, 20, 189–199.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi, M., Wei, S., & Wei, C. (2018). Identification of candidate olfactory genes in cicada Subpsaltria yangi by antennal transcriptome analysis. Comparative Biochemistry and Physiology Part d: Genomics and Proteomics, 28, 122–133.

    CAS  Google Scholar 

  • Quan, Q., Hu, X., Pan, B., Zeng, B., Wu, N., Fang, G., & Zhan, S. (2019). Draft genome of the cotton aphid Aphis gossypii. Insect Biochemistry and Molecular Biology, 105, 25–32.

    Article  CAS  PubMed  Google Scholar 

  • Robertson, H. M., Robertson, E. C. N., Walden, K. K. O., Enders, L. S., & Miller, N. J. (2019). The chemoreceptors and odorant binding proteins of the soybean and pea aphids. Insect Biochemistry and Molecular Biology, 105, 69–78.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, M. E., Sun, M., Lerner, M. R., & Vogt, R. G. (1997). Snmp-1, a novel membrane protein of olfactory neurons of the silk moth Antheraea polyphemus with homology to the CD36 family of membrane proteins. The Journal of Biological Chemistry, 272, 14792–14799.

    Article  CAS  PubMed  Google Scholar 

  • Rytz, R., Croset, V., & Benton, R. (2013). Ionotropic Receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochemistry and Molecular Biology, 43, 888–897.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt, H. R., & Benton, R. (2020). Molecular mechanisms of olfactory detection in insects: beyond receptors. Open Biology, 10, 200252. https://doi.org/10.1098/rsob.200252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soffan, A., Subandiyah, S., Makino, H., Watanabe, T., & Horiike, T. (2018). Evolutionary Analysis of the Highly Conserved Insect Odorant Coreceptor (Orco) Revealed a Positive Selection Mode, Implying Functional Flexibility. Journal of Insect Science, 18, 18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun, D., Huang, Y., Qin, Z., Zhan, H., Zhang, J., Liu, Y., & Yang, S. (2020). Identification of candidate olfactory genes in the antennal transcriptome of the stink bug Halyomorpha halys. Frontiers in Physiology, 11, 876.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian, Y., Chen, Z., Huang, X., Zhang, L., & Zhang, Z. (2020). Evaluation of Botanicals for Management of Piercing-Sucking Pests and the Effect on Beneficial Arthropod Populations in Tea Trees Camellia sinensis (L.) O. Kuntze (Theaceae). Journal of Insect Science, 20, 27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt, R. G., Miller, N. E., Litvack, R., Fandino, R. A., Sparks, J., Staples, J., & Dickens, J. C. (2009). The insect SNMP gene family. Insect Biochemistry and Molecular Biology, 39, 448–456.

    Article  CAS  PubMed  Google Scholar 

  • Wei, Q., Yu, H. Y., Niu, C. D., Yao, R., Wu, S. F., Chen, Z. M., & Gao, C. F. (2015). Comparison of insecticide susceptibilities of Empoasca vitis (Hemiptera: Cicadellidae) from three main tea-growing regions in China. Journal of Econonic Entomology, 108, 1251–1259.

    Article  CAS  Google Scholar 

  • Wicher, D. (2015). Olfactory Signaling in Insects. Progress in Molecular Biology and Translational Science, 130, 37–54.

    Article  CAS  PubMed  Google Scholar 

  • **ao, Y., Sun, L., Ma, X. Y., Dong, K., Liu, H. W., Wang, Q., & Zhang, Y. J. (2017). Identification and characterization of the distinct expression profiles of candidate chemosensory membrane proteins in the antennal transcriptome of Adelphocoris lineolatus (Goeze). Insect Molecular Biology, 26, 74–91.

    Article  CAS  PubMed  Google Scholar 

  • Xu, W., Papanicolaou, A., Zhang, H. J., & Anderson, A. (2016). Expansion of a bitter taste receptor family in a polyphagous insect herbivore. Scientific Reports, 6, 1–10.

    Google Scholar 

  • Xu, X. X., Cai, X. M., Bian, L., Luo, Z. X., Li, Z. Q., & Chen, Z. M. (2017). Does Background Odor in Tea Gardens Mask Attractants? Screening and Application of Attractants for Empoasca onukii Matsuda. Ecology and Behavior, 110, 2357–2363.

    CAS  Google Scholar 

  • Xu, W., Zhang, H., Liao, Y., & Papanicolaou, A. (2021). Characterization of sensory neuron membrane proteins (SNMPs) in cotton bollworm Helicoverpa armigera (Lepidoptera: Noctuidae). Insect Science, 28, 769–779.

    Article  CAS  PubMed  Google Scholar 

  • Yang, H., Dong, J., Sun, Y. L., Hu, Z., Lyu, Q. H., & Li, D. (2020a). Identification and expression profiles of candidate chemosensory receptors in Histia rhodope (Lepidoptera: Zygaenidae). PeerJ, 8, e10035.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, K., Gong, X. L., Li, G. C., Huang, L. Q., Ning, C., & Wang, C. Z. (2020b). A gustatory receptor tuned to the steroid plant hormone brassinolide in Plutella xylostella (Lepidoptera:Plutellidae). eLife, 9, e64114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • You, M., Yue, Z., He, W., Yang, X., Yang, G., **e, M., & Wang, J. (2013). A heterozygous moth genome provides insights into herbivory and detoxification. Natura Genetics, 45, 220–225.

    Article  CAS  Google Scholar 

  • Zeng, Y., Yang, Y. T., Wu, Q. J., Wang, S. L., **e, W., & Zhang, Y. J. (2019). Genome-wide analysis of odorant-binding proteins and chemosensory proteins in the sweet potato whitefly, Bemisia tabaci. Insect Science, 26, 620–634.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X. X., & Wang, G. R. (2020). Advances in research on the identification and function of ionotropic receptors in insects. Chinese Journal of Applied Entomology, 57, 1046–1055.

    Google Scholar 

  • Zhang, Z., Zhang, M., Yan, S., Wang, G., & Liu, Y. (2016). A female-biased odorant receptor from Apolygus lucorum (Meyer-Dür) tuned to some plant odors. International Journal of Molecular Sciences, 17, 1165.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y. N., Qian, J. L., Xu, J. W., Zhu, X. Y., Li, M. Y., Xu, X. X., & Sun, L. (2018). Identification of chemosensory genes based on the transcriptomic analysis of six different chemosensory genes organs in Spodoptera exigua. Frontiers in Physiology, 9, 432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, R. B., Liu, Y., Yan, S. C., & Wang, G. R. (2019). Identification and functional characterization of an odorant receptor in pea aphid, Acyrthosiphon pisum. Insect Science, 26, 58–67.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Q., Lan, R., Ji, D., Tan, Y., Zhou, X., Tan, X., & **, L. (2022). The Detection of Wolbachia in Tea Green Leafhopper (Empoasca onukii Matsuda) and Its Influence on the Host. Agriculture, 12, 36.

    Article  CAS  Google Scholar 

Download references

Funding

This work was financially supported by a grant from National Natural Science Foundation of China (32102303; 31501651), Natural Science Foundation of Shandong Province (ZR2020MC122; ZR2020QC132), Project of Laoshan District Tea Innovation Group (LSCG2022000017), Key Research and Development Program (2020ZDYF09), and Key Research and Development Program of Shandong Province (2022LZGCQY020).

Author information

Authors and Affiliations

Authors

Contributions

XYL and XZZ conceived research, performed the experiment and analyzed the data. XXX, YZ, RRZ, collected insects and prepared samples. ZQZ and XYL wrote the manuscript. ZQZ and YHZ secured funding and critically revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Yunhe Zhao or Zhengqun Zhang.

Ethics declarations

Competing interests

The authors have no relevant financial or nonfinancial interests to disclose.

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 565 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lun, X., Xu, X., Zhang, X. et al. Identification and expression profiles of candidate chemoreceptor genes in the tea leafhopper, Empoasca onukii Matsuda (Hemiptera: Cicadellidae). Phytoparasitica 51, 1073–1085 (2023). https://doi.org/10.1007/s12600-023-01107-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-023-01107-5

Keywords

Navigation