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Identification and characterization of olfactory genes in the parasitoid wasp Diadegma semiclausum (Hellén) (Hymenoptera: Ichneumonidae)

Published online by Cambridge University Press:  03 September 2021

Basman H. Al-Jalely
Affiliation:
Food Futures Institute, Murdoch University, Perth, WA6150, Australia College of Agricultural Engineering Sciences, University of Baghdad, Baghdad, Iraq
Penghao Wang
Affiliation:
Food Futures Institute, Murdoch University, Perth, WA6150, Australia
Yalin Liao
Affiliation:
Food Futures Institute, Murdoch University, Perth, WA6150, Australia
Wei Xu*
Affiliation:
Food Futures Institute, Murdoch University, Perth, WA6150, Australia
*
Author for correspondence: Wei Xu, Email: [email protected]

Abstract

Diadegma semiclausum is an important parasitoid wasp and widely used in the biological control of the diamondback moth, Plutella xylostella, one of the most destructive pests of cruciferous plants. Insect olfactory system is critical in guiding behaviors including feeding, mating, and oviposition, in which odorant binding proteins (OBPs) and odorant receptors (ORs) are two key components. However, limited attention has been paid to D. semiclausum olfactory genes. In this study, a transcriptome sequencing was performed on the RNA samples extracted from D. semiclausum male and female adult antennae. A total of 17 putative OBP and 67 OR genes were annotated and further compared to OBPs and ORs from P. xylostella, and other hemipteran parasitoid species. The expression patterns of D. semiclausum OBPs between male and female antennae were examined using reverse transcription polymerase chain reaction (RT-PCR) and quantitative real-time PCR. Six OBPs (DsemOBP 6, 7, 8, 9, 10, and 14) demonstrated significantly higher expression levels in females than in males, which may assist in female D. semiclausum host-seeking and oviposition behaviors. This study advances our understanding of the olfactory system of D. semiclausum at the molecular level and paves the way for future functional studies aiming at increasing the efficacy to control P. xylostella by using D. semiclausum.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Andrews, SF, Krueger, F, Seconds-Pichon, A, Biggins, F and Wingett, SF (2014) A quality control tool for high throughput sequence data. Babraham Bioinformatics.Google Scholar
Bai, SF, Cai, DZ, Li, X and Chen, XX (2009) Parasitic castration of Plutella xylostella larvae induced by polydnaviruses and venom of Cotesia vestalis and Diadegma semiclausum. Archives of Insect Biochemistry and Physiology 70, 3043.CrossRefGoogle ScholarPubMed
Bowers, WS, Nault, LR, Webb, RE and Dutky, SR (1972) Aphid alarm pheromone: isolation, identification, synthesis. Science (New York, N.Y.) 177, 11211122.CrossRefGoogle Scholar
Bukovinszky, T, Gols, R, Posthumus, MA, Vet, LE and Van Lenteren, JC (2005) Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellen). Journal of Chemical Ecology 31, 461480.CrossRefGoogle Scholar
Cai, L, Cheng, X, Qin, J, Xu, W and You, M (2020) Expression, purification and characterization of three odorant binding proteins from the diamondback moth, Plutella xylostella. Insect Molecular Biology 29, 531544.CrossRefGoogle ScholarPubMed
Cai, L, Zheng, L, Huang, Y, Xu, W and You, M (2021) Identification and characterization of odorant binding proteins in the diamondback moth, Plutella xylostella. Insect Science 28, 9871004.CrossRefGoogle ScholarPubMed
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, 327338.CrossRefGoogle ScholarPubMed
Dicke, M, Sabelis, MW, Takabayashi, J, Bruin, J and Posthumus, MA (1990) Plant strategies of manipulating predatorprey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16, 30913118.CrossRefGoogle ScholarPubMed
Dobin, A, Davis, CA, Schlesinger, F, Drenkow, J, Zaleski, C, Jha, S, Batut, P, Chaisson, M and Gingeras, TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics (Oxford, England) 29, 1521.CrossRefGoogle ScholarPubMed
Grabherr, MG, Haas, BJ, Yassour, M, Levin, JZ, Thompson, DA, Amit, I, Adiconis, X, Fan, L, Raychowdhury, R and Zeng, Q (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644652.CrossRefGoogle ScholarPubMed
Hatano, E, Kunert, G, Michaud, J and Weisser, WW (2008) Chemical cues mediating aphid location by natural enemies. European Journal of Entomology 105, 797806.CrossRefGoogle Scholar
Keil, TA (1984 a) Reconstruction and morphometry of the silkmoth olfactory hairs: a comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and A. pernyi (Insecta: Lepidoptera). Zoomorphologie 104, 8.Google Scholar
Keil, TA (1984 b) Surface coats of pore tubules and olfactory sensory dendrites of a silkmoth revealed by cationic markers. Tissue & Cell 16, 705717.CrossRefGoogle ScholarPubMed
Krieger, J and Breer, H (1999) Olfactory reception in invertebrates. Science (New York, N.Y.) 286, 720723.CrossRefGoogle ScholarPubMed
Larsson, MC, Hallberg, E, Kozlov, MV, Francke, W, Hansson, BS and Lofstedt, C (2002) Specialized olfactory receptor neurons mediating intra- and interspecific chemical communication in leafminer moths Eriocrania spp. (Lepidoptera: Eriocraniidae). Journal of Experimental Biology 205, 989998.CrossRefGoogle Scholar
Leal, WS (2003) Proteins that make sense. In Blomquist, GJ and Vogt, RG (eds), Insect Pheromone Biochemistry and Molecular Biology, the Biosynthesis and Detection of 464 Pheromone and Plant Volatiles. Elsevier Academic Press, pp. 447476.CrossRefGoogle Scholar
Leal, WS, Barbosa, RMR, Xu, W, Ishida, Y, Syed, Z, Latte, N, Chen, AM, Morgan, TI, Cornel, AJ and Furtado, A (2008) Reverse and conventional chemical ecology approaches for the development of oviposition attractants for Culex mosquitoes. PLoS One 3, e3045.CrossRefGoogle ScholarPubMed
Liu, NY, Xu, W, Papanicolaou, A, Dong, SL and Anderson, A (2014) Identification and 470 characterization of three chemosensory receptor families in the cotton bollworm 471 Helicoverpa armigera. BMC Genomics 15, 113.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods (San Diego, Calif.) 25, 402408.CrossRefGoogle Scholar
Pelletier, J and Leal, WS (2009) Genome analysis and expression patterns of odorant-binding proteins from the Southern House mosquito Culex pipiens quinquefasciatus. PLoS One 4, e6237.CrossRefGoogle ScholarPubMed
Pelosi, P, Iovinella, I, Zhu, J, Wang, GR and Dani, FR (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews 93, 184200.CrossRefGoogle ScholarPubMed
Robertson, HM and Wanner, KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Research 16, 13951403.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, 121136.CrossRefGoogle ScholarPubMed
Sato, K, Pellegrino, M, Nakagawa, T, Vosshall, LB and Touhara, K (2008) Insect olfactory receptors are heteromeric ligand-gated ion channels. Nature 452, 10021006.CrossRefGoogle ScholarPubMed
Syed, Z, Kopp, A, Kimbrell, DA and Leal, WS (2010) Bombykol receptors in the silkworm moth and the fruit fly. Proceedings of the National Academy of Sciences of the United States of America 107, 94369439.CrossRefGoogle ScholarPubMed
Tvedte, ES, Walden, KKO, McElroy, KE, Werren, JH, Forbes, AA, Hood, GR, Logsdon, JM, Feder, JL and Robertson, HM (2019) Genome of the parasitoid wasp Diachasma alloeum, an emerging model for ecological speciation and transitions to asexual reproduction. Genome Biology and Evolution 11, 27672773.CrossRefGoogle ScholarPubMed
Vandermoten, S, Francis, F, Haubruge, E and Leal, WS (2011) Conserved odorant-binding proteins from aphids and eavesdropping predators. PLoS One 6, e23608.CrossRefGoogle ScholarPubMed
Vogt, RG and Riddiford, LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293, 161163.CrossRefGoogle ScholarPubMed
Vosshall, LB, Amrein, H, Morozov, PS, Rzhetsky, A and Axel, R (1999) A spatial map of olfactory receptor expression in the Drosophila antennae. Cell 96, 725736.CrossRefGoogle Scholar
Wei, J, Wang, L, Zhu, J, Zhang, S, Nandi, O and Kang, L (2007) Plants attract parasitic wasps to defend themselves against insect pests by releasing hexenol. PLoS One, 0000852.CrossRefGoogle ScholarPubMed
Wicher, D, Schafer, R, Bauernfeind, R, Stensmyr, MC, Heller, R, Heinemann, SH and Hansson, BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452, 10071011.CrossRefGoogle ScholarPubMed
Wientjens, WHJM, Lakwijk, AC and van der Marel, T (1973) Alarm pheromone of grain aphids. Experientia 29, 658660.CrossRefGoogle Scholar
Xu, W and Anderson, A (2015) Carbon dioxide receptor genes in cotton bollworm Helicoverpa armigera. Naturwissenschaften 102, 11.CrossRefGoogle ScholarPubMed
Xu, W and Liao, Y (2017) Identification and characterization of aldehyde oxidases (AOXs) in the cotton bollworm. The Science of Nature 104, 94.CrossRefGoogle ScholarPubMed
Xu, P, Atkinson, R, Jones, DN and Smith, DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193200.CrossRefGoogle ScholarPubMed
Xu, W, Liu, N, Liao, Y and Anderson, A (2017) Molecular characterization of sugar taste receptors in the cotton bollworm Helicoverpa armigera. Genome 60, 10371044.CrossRefGoogle ScholarPubMed
You, M, Yue, Z, He, W, Yang, X, Yang, G, Xie, M, Zhan, D, Baxter, SW, Vasseur, L, Gurr, GM, Douglas, CJ, Bai, J, Wang, P, Cui, K, Huang, S, Li, X, Zhou, Q, Wu, Z, Chen, Q, Liu, C, Wang, B, Li, X, Xu, X, Lu, C, Hu, M, Davey, JW, Smith, SM, Chen, M, Xia, X, Tang, W, Ke, F, Zheng, D, Hu, Y, Song, F, You, Y, Ma, X, Peng, L, Zheng, Y, Liang, Y, Chen, Y, Yu, L, Zhang, Y, Liu, Y, Li, G, Fang, L, Li, J, Zhou, X, Luo, Y, Gou, C, Wang, J, Wang, J, Yang, H and Wang, J (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nature Genetics 45, 220225.CrossRefGoogle ScholarPubMed
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