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Antennal transcriptome analysis and candidate olfactory genes in Crematogaster rogenhoferi

Published online by Cambridge University Press:  11 March 2021

Xiang Zhou ,
Jixing Guo Open the ORCID record for Jixing Guo [Opens in a new window] ,
Mingxia Zhang ,
Chunxiu Bai ,
Zheng Wang  and
Zhidong Li
Xiang Zhou
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
Jixing Guo*
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
Mingxia Zhang
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
Chunxiu Bai
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
Zheng Wang
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
Zhidong Li
Affiliation:
College of Plant Protection, Hainan University, Haikou570228, China Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests (Ministry of Education), Hainan University, Haikou570228, China
*
Author for correspondence: Jixing Guo, Email: guojixing@hainanu.edu.cn
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Abstract

Crematogaster rogenhoferi (Hymenoptera: Formicidae), an omnivorous ant, is one of the dominant predatory natural enemies of a soft scale pest, Parasaissetia nigra Nietner (Homoptera: Coccidae), and can effectively control P. nigra populations in rubber forests. Olfaction plays a vital role in the process of predation. However, the information about the molecular mechanism of olfaction-evoked behaviour in C. rogenhoferi is limited. In this study, we conducted antennal transcriptome analysis to identify candidate olfactory genes. We obtained 53,892 unigenes, 16,185 of which were annotated. Based on annotations, we identified 49 unigenes related to chemoreception, including four odourant-binding proteins, three chemosensory proteins, 37 odourant receptors, two odourant ionotropic receptors and three sensory neuron membrane proteins. This is the first report on the molecular basis of the chemosensory system of C. rogenhoferi. The findings provide a basis for elucidating the molecular mechanisms of the olfactory-related behaviours of C. rogenhoferi, which would facilitate a better application of C. rogenhoferi as a biological control agent.

Keywords

Antennal transcriptomeCrematogaster rogenhoferiolfactory genessequence analysis
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 4 , August 2021 , pp. 464 - 475
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abuin, L, Bargeton, B, Ulbrich, MH, Isacoff, EY, Kellenberger, S and Benton, AR (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69, 44–60.CrossRefGoogle ScholarPubMed
Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Ashburner, M, Ball, CA, Blake, JA, Botstein, D, Butler, H, Cherry, JM, Davis, AP, Dolinski, K, Dwight, SS, Eppig, JT, Harris, MA, Hill, DP, Issel-Tarver, L, Kasarskis, A, Lewis, S, Matese, JC, Richardson, JE, Ringwald, M, Rubin, GM and Sherlock, G (2000) Gene ontology: tool for the unification of biology. Nature Genetics 25, 25–9.CrossRefGoogle ScholarPubMed
Bengtsson, JM, Trona, F, Montagné, N, Anfora, G, Ignell, R, Witzgall, P and Jacquin-Joly, E (2012) Putative chemosensory receptors of the codling moth, Cydia Pomonella, identified by antennal transcriptome analysis. PLoS One 7, e31620.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
Benton, R, Vannice, KS, Gomez-Diaz, C and Vosshall, LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162.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
Calvello, M, Brandazza, A, Navarrini, A, Dani, FR, Turillazzi, S, Felicioli, A and Pelosi, P (2005) Expression of odorant-binding proteins and chemosensory proteins in some Hymenoptera. Insect Biochemistry and Molecular Biology 35, 297–307.CrossRefGoogle ScholarPubMed
Chen, P (2014) Occurrence regularities and control strategies of Parasaissetia nigra Nietner in Yunnan. Applicable Technologies for Rural Areas 02, 38–39.Google Scholar
Clyne, PJ, Warr, CG, Freeman, MR, Lessing, D, Kim, J and Carlson, JR (1999) A novel family of divergent seven transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327–338.CrossRefGoogle ScholarPubMed
Croset, V, Rytz, R, Cummins, SF, Budd, A, Brawand, D, Kaessmann, H, Gibson, TJ and Benton, R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genetics 6, e1001064.CrossRefGoogle ScholarPubMed
Deng, Y, Li, J, Wu, S, Zhu, Y, Chen, Y and He, F (2006) Integrated nr Database in protein annotation system and its localization. Computer Engineering 32, 71–76.Google Scholar
Eddy, SR (1998) Profile hidden Markov models. Bioinformatics 14, 755–763.CrossRefGoogle ScholarPubMed
Engsontia, P, Sangket, U, Robertson, HM and Satasook, C (2015) Diversification of the ant odorant receptor gene family and positive selection on candidate cuticular hydrocarbon receptors. BMC Research Notes 8, 380.CrossRefGoogle ScholarPubMed
Finn, RD, Bateman, A, Clements, J, Coggill, P, Eberhardt, RY, Eddy, SR, Heger, A, Hetherington, K, Holm, L, Mistry, J, Sonnhammer, EL, Tate, J and Punta, M (2014) Pfam: the protein families database. Nucleic Acids Research 42, D222–30.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 pheromone-sensitive hairs of moths. Chemical Senses 33, 291–299.CrossRefGoogle ScholarPubMed
Gong, DP, Zhang, HJ, Zhao, P, Xia, QY and Xiang, ZH (2009) The odorant binding protein gene family from the genome of silkworm, Bombyx mori. BMC Genomics 10, 332.CrossRefGoogle ScholarPubMed
Gu, SH, Wang, SP, Zhang, XY, Wu, KM, Guo, YY, Zhou, JJ and Zhang, YJ (2011) Identification and tissue distribution of odorant binding protein genes in the lucerne plant bug Adelphocoris lineolatus (Goeze). Insect Biochemistry and Molecular Biology 41, 254–263.CrossRefGoogle Scholar
Gu, SH, Zhou, JJ, Gao, S, Wang, DH, Li, XC, Guo, YY and Zhang, YJ (2015) Identification and comparative expression analysis of odorant binding protein genes in the tobacco cutworm Spodoptera litura. Scientific Reports 5, 13800.CrossRefGoogle ScholarPubMed
Hallem, EA, Dahanukar, A and Carlson, JR (2006) Insect odor and taste receptors. Annual Review of Entomology 51, 113–135.CrossRefGoogle ScholarPubMed
Hildebrand, JG (1995) Analysis of chemical signals by nervous systems. Proceedings of the National Academy of Sciences 92, 67–74.CrossRefGoogle ScholarPubMed
Hildebrand, JG and Shepherd, GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annual Review of Neuroscience 20, 595–631.CrossRefGoogle ScholarPubMed
Hu, P, Wang, J, Cui, M, Tao, J and Luo, Y (2016) Antennal transcriptome analysis of the Asian longhorned beetle Anoplophora glabripennis. Scientific Reports 6, 1–12.Google ScholarPubMed
Huang, YG, Wei, JS, Xi, FS and Liu, Z (1984) A preliminary report on the investigation and study of Crematogaster rogenhoferi. Guangxi Forestry Science 1, 19–22.Google Scholar
Ishida, Y, Chiang, V and Leal, WS (2002) Protein that makes sense in the Argentine ant. Naturwissenschaften 89, 505–507.CrossRefGoogle ScholarPubMed
Kanehisa, M, Araki, M, Goto, S, Hattori, M, Hirakawa, M, Itoh, M, Katayama, T, Kawashima, S, Okuda, S, Tokimatsu, T and Yamanishi, Y (2007) KEGG For linking genomes to life and the environment. Nucleic acids Research 36, D480–D484.CrossRefGoogle ScholarPubMed
Koonin, EV, Fedorova, ND, Jackson, JD, Jacobs, AR, Krylov, DM, Makarova, KS, Mazumder, R, Mekhedov, SL, Nikolskaya, AN and Rao, BS (2004) A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome biology 5, R7.CrossRefGoogle ScholarPubMed
Krieger, MJB and Ross, KG (2002) Identification of a major gene regulating complex social behavior. Science (New York, N.Y.) 11, 328–332.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
McKenzie, SK, Oxley, PR and Kronauer, DJC (2014) Comparative genomics and transcriptomics in ants provide new insights into the evolution and function of odorant binding and chemosensory proteins. BMC Genomics 15, 718.CrossRefGoogle ScholarPubMed
Pelosi, P and Maida, R (1995) Odorant-binding proteins in insects. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 111, 503–514.CrossRefGoogle ScholarPubMed
Pelosi, P, Zhou, JJ, Ban, LP and Calvello, M (2006) Soluble proteins in insect chemical communication. Cellular and Molecular Life Sciences CMLS 63, 1658–1676.CrossRefGoogle ScholarPubMed
Pelosi, P, Iovinella, I, Felicioli, A and Dani, FR (2014) Soluble proteins of chemical communication: an overview across arthropods. Frontiers in Physiology 5, 320.CrossRefGoogle ScholarPubMed
Pertea, G, Huang, X, Liang, F, Antonescu, V, Sultana, R, Karamycheva, S, Lee, Y, White, J, Cheung, F and Parvizi, B (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19, 651–652.CrossRefGoogle ScholarPubMed
Poivet, E, Gallot, A, Montagné, N, Glaser, N, Legeai, F and Jacquinjoly, E (2013) Acomparison of the olfactory gene repertoires of adults and larvae in the noctuid moth Spodoptera littoralis. PLoS One 8, e60263.CrossRefGoogle Scholar
Richard, FJ and Hunt, JH (2013) Intracolony chemical communication in social insects. Insectes Sociaux 60, 275–291.CrossRefGoogle Scholar
Robertson, HM, Gadau, J and Wanner, KW (2010) The insect chemoreceptor superfamily of the parasitoid jewel wasp Nasonia vitripennis. Insect Molecular Biology 19, 121–136.CrossRefGoogle ScholarPubMed
Rogers, ME, Sun, M, Lerner, MR and Vogt, RG (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. Journal of Biological Chemistry 272, 14792–14799.CrossRefGoogle ScholarPubMed
Rogers, ME, Krieger, J and Vogt, RG (2001) Antennal SNMPs (sensory neuron membrane proteins) of Lepidoptera define a unique family of invertebrate CD36-like proteins. Journal of Neurobiology 49, 47–61.CrossRefGoogle ScholarPubMed
Sun, H, Song, Y, Du, J, Wang, X and Cheng, Z (2016) Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Athetis dissimilis (Lepidoptera: Noctuidae). Applied entomology and zoology, 51, 409–420.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Vieira, FG and Rozas, J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome biology and evolution 3, 476–490.CrossRefGoogle ScholarPubMed
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, Q and Zhou, X (2012) Preliminary research for artificial raising and release of gremastogaste rogenhoferi. Guangdong Agricultural Sciences 39, 98–100.Google Scholar
Wei, JN and Yu, XW (1998) A preliminary study on the diversity and control evaluation of natural enemies of coffee stem borers, Xylotrechus Quardripes And Acalolepta cervinus (Coleoptera:Cerambycidae) in Simao region, Yunnan Province. Chinese Biodiversity 6, 248–252.Google Scholar
Zhang, J, Liu, Y, Walker, WB, Dong, SL and Wang, GR (2015) Identification and localization of two sensory neuron membrane proteins from Spodoptera Litura (Lepidoptera: Noctuidae). Insect Science 22, 399–408.CrossRefGoogle Scholar
Zhang, L, Du, B, Qiu, B and Wang, H (2017) Study on potency of controlling on Crematogaster Rogenhoferi to Parasaissetia Nigra Nietner. International Symposium on Intelligence Computation and Applications 874, 280–289.Google Scholar
Zhou, JJ (2010) Odorant-binding proteins in insects. Vitamins & Hormones 83, 241–272.CrossRefGoogle ScholarPubMed
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