Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-24T10:25:40.844Z Has data issue: false hasContentIssue false
  • English
  • Français

Identification and analysis of chemosensory genes encoding odorant-binding proteins, chemosensory proteins and sensory neuron membrane proteins in the antennae of Lissorhoptrus oryzophilus

Published online by Cambridge University Press:  30 September 2021

Yu Pan ,
Xinxin Zhang ,
Zhun Wang ,
Lizhong Qi ,
Xinsheng Zhang ,
Juhong Zhang  and
Jinghui Xi Open the ORCID record for Jinghui Xi [Opens in a new window]
Yu Pan
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China
Xinxin Zhang*
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China Department of Plant Protection, College of Agriculture, Northeast Agricultural University, Harbin, China
Zhun Wang
Affiliation:
Changchun Customs Technology Center, Changchun, China
Lizhong Qi
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China
Xinsheng Zhang*
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China
Juhong Zhang*
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China
Jinghui Xi*
Affiliation:
College of Plant Science, Jilin University, Changchun 130062, PR China
*
Author for correspondence: Jinghui Xi, Email: jhxi1965@jlu.edu.cn; Juhong Zhang, Email: zhjhqhd@126.com
Author for correspondence: Jinghui Xi, Email: jhxi1965@jlu.edu.cn; Juhong Zhang, Email: zhjhqhd@126.com
Author for correspondence: Jinghui Xi, Email: jhxi1965@jlu.edu.cn; Juhong Zhang, Email: zhjhqhd@126.com
Author for correspondence: Jinghui Xi, Email: jhxi1965@jlu.edu.cn; Juhong Zhang, Email: zhjhqhd@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The rice water weevil, Lissorhoptrus oryzophilus Kuschel (Coleoptera: Curculionidae), is a destructive pest that causes damage to rice crops worldwide. The olfactory system is critical for host or mate location by weevils, but only limited information about the molecular mechanism of olfaction-related behaviour has been reported in this insect. In this study, we conducted SMRT-seq transcriptome analysis and obtained 54,378 transcripts, 38,706 of which were annotated. Based on these annotations, we identified 40 candidate chemosensory genes, including 31 odorant-binding proteins (OBPs), six chemosensory proteins (CSPs) and three sensory neuron membrane proteins (SNMPs). Phylogenetic analysis showed that LoryOBPs, LoryCSPs and LorySNMPs were distributed in various clades. The results of tissue expression patterns indicated that LoryOBPs were highly abundant in the antennae, whereas LoryCSPs were highly abundant not only in the antennae but also in the abdomen, head and wings. Our findings substantially expand the gene database of L. oryzophilus and may serve as a basis for identifying novel targets to disrupt key olfactory genes, potentially providing an eco-friendly strategy to control this pest in the future.

Keywords

Chemosensory geneL. oryzophilustissue expressionSMRT-seq
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 3 , June 2022 , pp. 287 - 297
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Aghaee, M and Godfrey, LD (2014) A century of rice water weevil (Coleoptera: Curculionidae): a history of research an management with an emphasis on the United States. Journal of Integrated Pest Management 5, 1–14.CrossRefGoogle Scholar
Andersson, MN, Grosse-Wilde, E, Keeling, CI, Bengtsson, JM, Yuen, MMS, Li, M, Hillbur, Y, Bohlmann, J, Hansson, BS and 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.CrossRefGoogle Scholar
Angeli, S, Ceron, F, Scaloni, A, Monti, M, Monteforti, G, Minnocci, A, Petacchi, R and Pelosi, P (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. European Journal of Biochemisty 262, 745–754.CrossRefGoogle ScholarPubMed
Antony, B, Soffan, A, Jakse, J, Abdelazim, MM, Aldosari, SA, Aldawood, AS and Pain, A (2016) 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 Genomics 17, 69.CrossRefGoogle ScholarPubMed
Benton, R, Vannice, KS and Vosshall, LB (2007) An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature 450, 289–293.CrossRefGoogle ScholarPubMed
Bin, SY, Qu, MQ, Pu, XH, Wu, ZZ and Lin, JT (2017) Antennal transcriptome and expression analyses of olfactory genes in the sweet potato weevil Cylas formicarius. Scientific Reports 7, 11073.CrossRefGoogle ScholarPubMed
Birkett, MA, Agelopoulos, N, Jensen, KMV, Jespersen, JB, Pickett, JA, Prijs, HJ, Thomas, G, Trapman, JJ, Wadhams, LJ and Woodcock, CM (2004) The role of volatile semiochemicals in mediating host locationand selection by nuisance and disease-transmitting cattle flies. Medical and Veterinary Entomology 18, 313–322.CrossRefGoogle Scholar
Carey, AF, Wang, GR, Su, CY, Zwiebel, LJ and Carlson, JR (2010) Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464, 66–71.CrossRefGoogle ScholarPubMed
Chen, H, Chen, ZM and Zhou, YS (2005) Rice water weevil (Coleoptera: Curculionidae) in mainland China: invasion, spread and control. Crop Protection 24, 695–702.CrossRefGoogle Scholar
Chen, GL, Pan, YF, Ma, YF, Wang, J, He, M and He, P (2018) Binding affinity characterization of an antennae-enriched chemosensory protein from the white-backed planthopper, Sogatella furcifera (Horvath), with host plant volatiles. Pesticide Biochemistry and Physiology 152, 1–7.CrossRefGoogle Scholar
Fleischer, J, Pregitzer, P, Breer, H and Krieger, J (2018) Access to the odor world: olfactory receptors and their role for signal transduction in insects. Cellular and Molecular Sciences 75, 485–508.CrossRefGoogle Scholar
Forêt, S, Wanner, KW and Maleszka, R (2007) Chemosensory proteins in the honey bee: insights from the annotated genome, comparative analyses and expressional profiling. Insect Biochemistry and Molecular Biology 37, 19–28.CrossRefGoogle ScholarPubMed
Forstner, M, Gohl, T, Gondesen, I, Raming, K, Breer, H and Krieger, J (2008) Differential expression of SNMP-1 and SNMP-2 proteins in pheromonesensitive hairs of moths. Chemical Senses 33, 291–299.CrossRefGoogle Scholar
Hua, JF, Zhang, S, Cui, JJ, Wang, DJ, Wang, CY, Luo, JY, Lv, LM and Ma, Y (2013) Functional characterizations of one odorant binding protein and three chemosensory proteins from Apolygus lucorum (Meyer-Dur) (Hemiptera: Miridae) legs. Journal of Insect Physiology 59, 690–696.CrossRefGoogle ScholarPubMed
Ingham, VA, Anthousi, A, Douris, V, Harding, NJ, Lycett, G, Morris, M, Vontas, J and Ranson, H (2020) A sensory appendage protein protects malaria vectors from pyrethroids. Nature 577, 376–380.CrossRefGoogle ScholarPubMed
Jacquin-Joly, E, Vogt, RG, Francois, MC and Nagnan-Le Meillour, P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chemical Senses 26, 833–844.CrossRefGoogle ScholarPubMed
Jin, X, Ha, TS and Smith, DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proceedings of the National Academy of Sciences of the United States America 105, 10996–11001.CrossRefGoogle ScholarPubMed
Kanehisa, M, Goto, S, Kawashima, S, Okuno, Y and Hattori, M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research 32, D277–D280.CrossRefGoogle ScholarPubMed
Kitabayashi, AN, Arai, T, Kubo, T and Natori, S (1998) Molecular cloning of cDNA for p10, a novel protein that increases in regenerating legs of Periplaneta americana (American cockroach). Insect Biochemistry and Molecular Biology 28, 785–790.CrossRefGoogle Scholar
Lagarde, A, Spinelli, S, Qiao, HL, Tegoni, M, Pelosi, P and Cambillau, C (2011) Crystal structure of a novel type of odorant-binding protein from Anopheles gambiae, belonging to the C-plus class. Biochemical Journal 437, 423–430.CrossRefGoogle Scholar
Leal, WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology 58, 373–391.CrossRefGoogle ScholarPubMed
Li, XM, Zhu, XY, Wang, ZQ, Wang, Y, He, P, Chen, G, Sun, L, Deng, DG and Zhang, YN (2015) Candidate chemosensory genes identified in Colaphellus bowringi by antennal transcriptome analysis. BMC Genomics 16, 1028.CrossRefGoogle ScholarPubMed
Li, LL, Xu, JW, Yao, WC, Yang, HH, Dewer, Y, Zhang, F, Zhu, XY and Zhang, YN (2021) Chemosensory genes in the head of Spodoptera litura larvae. Bulletin of Entomological Research 111, 454–463.CrossRefGoogle ScholarPubMed
Liu, R, He, X, Lehane, S, Lehane, M, Hertz-Fowler, C, Berriman, M, Field, LM and Zhou, JJ (2012) Expression of chemosensory proteins in the tsetse fly Glossina morsitans morsitans is related to female host-seeking behaviour. Insect Molecular Biology 21, 41–48.CrossRefGoogle ScholarPubMed
Mao, XZ, Cai, T, Olyarchuk, JG and Wei, LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics (Oxford, England) 21, 3787–3793.CrossRefGoogle Scholar
Palrang, AT, Grigarick, AA, Oraze, MJ and Hesler, LS (1994) Association of levee vegetation to rice water weevil (Coleoptera: Curculionidae) infestation in California rice. Journal of Economic Entomology 87, 1701–1706.CrossRefGoogle Scholar
Pelosi, P, Zhou, JJ, Ban, LP and Calvello, M (2006) Soluble proteins in insect chemical communication. Cellular and Molecular Sciences 63, 1658–1676.CrossRefGoogle ScholarPubMed
Pelosi, P, Iovinella, I, Felicioli, A and Dani, FD (2014) Soluble proteins of chemical communication: an overview across arthropods. Frontiers in Physiology 5, 320.CrossRefGoogle ScholarPubMed
Pelosi, P, Iovinella, I, Zhu, J, Wang, GR and Dani, FR (2018 a) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews 93, 184–200.CrossRefGoogle ScholarPubMed
Pelosi, P, Zhu, J and Knoll, W (2018 b) Odorant-binding proteins as sensing elements for odour monitoring. Sensors 18, 3248.CrossRefGoogle ScholarPubMed
Pregitzer, P, Schubert, M, Breer, H, Hansson, BS, Sachse, S and Krieger, J (2012) Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Frontiers in Cellular Neuroscience 6, 42.CrossRefGoogle ScholarPubMed
Pregitzer, P, Greschista, M, Breer, H and Krieger, J (2014) The sensory neurone membrane protein SNMP1 contributes to the sensitivity of a pheromone detection system. Insect Molecular Biology 23, 733–742.CrossRefGoogle Scholar
Robertson, HM, Martos, R, Sears, CR, Todres, EZ, Walden, KKO and Nardi, JB (1999) Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antennae. Insect Molecular Biology 8, 501–518.CrossRefGoogle ScholarPubMed
Saito, T, Hirai, K and Way, MO (2005) The rice water weevil, Lissorhoptrus oryzophilus Kuschel (Coleoptera: curculionidae). Applied Entomology and Zoology 40, 31–39.CrossRefGoogle Scholar
Stensmyr, MC, Dweck, HKM, Farhan, A, Ibba, I, Strutz, A, Mukunda, L, Linz, J, Grabe, V, Steck, K, Lavista-Llanos, S, Wicher, D, Sachse, S, Knaden, M, Becher, PG, Seki, Y and Hansson, BS (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151, 1345–1357.CrossRefGoogle ScholarPubMed
Swarup, S, Morozova, TV, Sridhar, S, Nokes, M and Anholt, RRH (2014) Modulation of feeding behavior by odorant-binding proteins in Drosophila melanogaster. Chemical Senses 39, 125–132.CrossRefGoogle ScholarPubMed
Thompson, RA and Quisenberry, SS (1995) Rice plant density effect on rice water weevil (Coleoptera: Curculionidae) infestation. Environmental Entomology 24, 19–23.CrossRefGoogle Scholar
Tindall, KV and Stout, MJ (2003) Use of common weeds of rice as hosts for the rice water weevil (Coleoptera: Curculionidae). Environmental Entomology 32, 1227–1233.CrossRefGoogle Scholar
Touhara, K and Vosshall, LB (2009) Sensing odorants and pheromones with chemosensory receptors. Annual Review of Physiology 71, 307–332.CrossRefGoogle ScholarPubMed
Tsitsanou, KE, Drakou, CE, Thireou, T, Gruber, AV, Kythreoti, G, Azem, A, Fessas, D, Eliopoulos, E, Iatrou, K and Zographos, SE (2013) Crystal and solution studies of the ‘ Plus-C ‘ odorant-binding protein 48 from anopheles gambiae control of binding specificity through three-dimensional domain swapping. Journal of Biological Chemistry 288, 33427–33438.CrossRefGoogle Scholar
Vogt, RG, Miller, NE, Litvack, R, Fandino, RA, Sparks, J, Staples, J, Friedman, R and Dickens, JC (2009) The insect SNMP gene family. Insect Biochemistry and Molecular Biology 39, 448–456.CrossRefGoogle ScholarPubMed
Wang, B, Guan, L, Zhong, T, Li, KB, Yin, J and Cao, YZ (2013) Potential cooperations between odorant-binding proteins of the scarab beetle Holotrichia oblita Faldermann (Coleoptera: Scarabaeidae). PLoS One 8, e84795.CrossRefGoogle Scholar
Wang, S, Liu, Y, Zhou, JJ, Yi, JK, Pan, Y, Wang, J, Zhang, XX, Wang, JX, Yang, S and Xi, JH (2018) Identification and tissue expression profiling of candidate UDP-glycosyltransferase genes expressed in Holotrichia parallela motschulsky antennae. Bulletin of Entomological Research 108, 807–816.CrossRefGoogle ScholarPubMed
Yang, S, Zhang, XX, Wang, JX, Wang, S, Pan, Y, Zhang, JH and Xi, JH (2018) Identification and analysis of up-regulated proteins in Lissorhoptrus oryzophilus adults for rapid, cold hardening. Gene 642, 9–15.CrossRefGoogle ScholarPubMed
Yi, JK, Yang, S, Wang, S, Wang, J, Zhang, XX, Liu, Y and Xi, JH (2018) Identification of candidate chemosensory receptors in the antennal transcriptome of the large black chafer Holotrichia parallela Motschulsky (Coleoptera: Scarabaeidae). Comparative Biochemistry and Physiology D-Genomics & Proteomics 28, 63–71.CrossRefGoogle Scholar
Yin, J, Wang, CQ, Fang, CQ, Zhang, S, Cao, YZ, Li, KB and Leal, WS (2019) Functional characterization of odorant-binding proteins from the scarab beetle Holotrichia oblita based on semiochemical-induced expression alteration and gene silencing. Insect Biochemistry and Molecular Biology 104, 11–19.CrossRefGoogle ScholarPubMed
Yuan, X, Jiang, YD, Wang, GY, Yu, H, Zhou, WW, Liu, S, Yang, MF, Cheng, J, Gurr, GM, Way, MO and Zhu, ZR (2016) Odorant-binding proteins and chemosensory proteins from an invasive pest Lissorhoptrus oryzophilus (Coleoptera: Curculionidae). Environmental Entomology 45, 1276–1286.CrossRefGoogle Scholar
Zhang, YN, Ye, ZF, Yang, K and Dong, SL (2014) Antenna-predominant and male-biased CSP19 of Sesamia Inferens is able to bind the female sex pheromones and host plant volatiles. Gene 536, 279–286.CrossRefGoogle ScholarPubMed
Zhang, XX, Yang, S, Zhang, JH, Wang, X, Wang, S, Liu, MN and Xi, JH (2019) Identification and expression analysis of candidate chemosensory receptors based on the antennal transcriptome of Lissorhoptrus oryzophilus. Comparative Biochemistry and Physiology D-Genomics & Proteomics 30, 133–142.CrossRefGoogle ScholarPubMed
Zhuang, X, Wang, Q, Wang, B, Zhong, T, Cao, Y, Li, K and Yin, J (2014) Prediction of the key binding site of odorant-binding protein of Holotrichia oblita Faldermann (Coleoptera: Scarabaeida). Insect Molecular Biology 23, 381–390.Google Scholar
Supplementary material: File

Pan et al. supplementary material

Pan et al. supplementary material

Download Pan et al. supplementary material(File)
File 1.3 MB