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AlepPBP2, but not AlepPBP3, may involve in the recognition of sex pheromones and maize volatiles in Athetis lepigone

Published online by Cambridge University Press:  24 February 2022

Hui-Hui Yang*
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Ji-Wei Xu
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Xiao-Qing Zhang
Affiliation:
Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, College of Plant Protection, Nanjing Agricultural University, Nanjing, China
Jian-Rong Huang
Affiliation:
Henan Key Laboratory of Crop Pest Control, MOA's Regional Key Lab of Crop IPM in Southern Part of Northern China, Institute of Plant Protection, Henan Academy of Agricultural Sciences, Zhengzhou, China
Lu-Lu Li
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Wei-Chen Yao
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Pan-Pan Zhao
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Dong Zhang
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Jia-Yi Liu
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China College of Information, Huaibei Normal University, Huaibei, China
Youssef Dewer
Affiliation:
Phytotoxicity Research Department, Central Agricultural Pesticide Laboratory, Agricultural Research Center, 7 Nadi El-Seid Street, Dokki 12618, Giza, Egypt
Xiu-Yun Zhu
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Xiao-Ming Li
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
Ya-Nan Zhang
Affiliation:
Anhui Province Key Laboratory of Pollutant Sensitive Materials and Environmental Remediation, Anhui Provincial Engineering Laboratory for Efficient Utilization of Featured Resource Plants, College of Life Sciences, Huaibei Normal University, Huaibei, China
*
Author for correspondence: Ya-Nan Zhang, Email: [email protected]; Xiu-Yun Zhu, Email: [email protected]; Xiao-Ming Li, Email: [email protected]

Abstract

Athetis lepigone Möschler (Lepidoptera, Noctuidae) is a common maize pest in Europe and Asia. However, there is no long-term effective management strategy is available yet to suppress its population. Adults rely heavily on olfactory cues to locate their optimal host plants and oviposition sites. Pheromone-binding proteins (PBPs) are believed to be responsible for recognizing and transporting different odorant molecules to interact with receptor membrane proteins. In this study, the ligand-binding specificities of two AlepPBPs (AlepPBP2 and AlepPBP3) for sex pheromone components and host plant (maize) volatiles were measured by fluorescence ligand-binding assay. The results demonstrated that AlepPBP2 had a high affinity with two pheromones [(Z)-7-dodecenyl acetate, Ki = 1.11 ± 0.1 μM, (Z)-9-tetradecenyl acetate, Ki = 1.32 ± 0.15 μM] and ten plant volatiles, including (-)-limonene, α-pinene, myrcene, linalool, benzaldehyde, nonanal, 2-hexanone, 3-hexanone, 2-heptanone and 6-methyl-5-hepten-2-one. In contrast, we found that none of these chemicals could bind to AlepPBP3. Our results clearly show no significant differences in the functional characterization of the binding properties between AlepPBP2 and AlepPBP3 to sex pheromones and host plant volatiles. Furthermore, molecular docking was employed for further detail on some crucial amino acid residues involved in the ligand-binding of AlepPBP2. These findings will provide valuable information about the potential protein binding sites necessary for protein-ligand interactions which appear as attractive targets for the development of novel technologies and management strategies for insect pests.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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Footnotes

*

They contributed equally to this work.

References

Abraham, D, Löfstedt, C and Picimbon, J-F (2005) Molecular characterization and evolution of pheromone binding protein genes in Agrotis moths. Insect Biochemistry and Molecular Biology 35, 11001111.CrossRefGoogle ScholarPubMed
Binder, BF, Robbins, JC and Wilson, RL (1995) Chemically mediated ovipositional behaviors of the European corn borer, Ostrinia nubilalis(Lepidoptera: Pyralidae). Journal of Chemical Ecology 21, 13151327.CrossRefGoogle Scholar
Caballero-Vidal, G, Bouysset, C, Gevar, J, Mbouzid, H, Nara, C, Delaroche, J, Golebiowski, J, Montagne, N, Fiorucci, S and Jacquin-Joly, E (2021) Reverse chemical ecology in a moth: machine learning on odorant receptors identifies new behaviorally active agonists. Cellular and Molecular Life Sciences 78, 65936603.CrossRefGoogle Scholar
Campanacci, V, Krieger, J, Bette, S, Sturgis, JN, Lartigue, A, Cambillau, C, Breer, H and Tegoni, M (2001) Revisiting the specificity of Mamestra brassicae and Antheraea polyphemus pheromone-binding proteins with a fluorescence binding assay. Journal of Biological Chemistry 276, 2007820084.CrossRefGoogle ScholarPubMed
Chang, H, Liu, Y, Yang, T, Pelosi, P, Dong, S and Wang, G (2015) Pheromone binding proteins enhance the sensitivity of olfactory receptors to sex pheromones in Chilo suppressalis. Scientific Reports 5, 1309313104.CrossRefGoogle ScholarPubMed
Chisholm, MD, Underhill, EW and Steck, WF (1979) Field trapping of the diamondback moth Plutella xylostella using synthetic sex attractants. Environmental Entomology 8, 516518.CrossRefGoogle Scholar
Choo, YM, Xu, P, Hwang, JK, Zeng, F, Tan, K, Bhagavathy, G, Chauhan, KR and Leal, WS (2018) Reverse chemical ecology approach for the identification of an oviposition attractant for Culex quinquefasciatus. Proceedings of the National Academy of Sciences of the United States of America 115, 714719.CrossRefGoogle ScholarPubMed
Collignon, RM, Swift, IP, Zou, Y, McElfresh, JS, Hanks, LM and Millar, JG (2016) The influence of host plant volatiles on the attraction of longhorn beetles to pheromones. Journal of Chemical Ecology 42, 215229.CrossRefGoogle ScholarPubMed
Curkovic, T and Ferrera, C (2012) Female calling and male flight orientation and searching behaviors in Callisphyris apicicornis: evidence for a female-produced sex attractant pheromone. Cienc Investig Agrar 39, 147158.CrossRefGoogle Scholar
Damberger, FF, Michel, E, Ishida, Y, Leal, WS and Wuthrich, K (2013) Pheromone discrimination by a pH-tuned polymorphism of the Bombyx mori pheromone-binding protein. Proceedings of the National Academy of Sciences of the United States of America 110, 1868018685.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
Dong, K, Sun, L, Liu, JT, Gu, SH, Zhou, JJ, Yang, RN, Dhiloo, KH, Gao, XW, Guo, YY and Zhang, YJ (2017a) RNAi-Induced electrophysiological and behavioral changes reveal two pheromone binding proteins of Helicoverpa armigera involved in the perception of the main sex pheromone component Z11-16:Ald. Journal of Chemical Ecology 43, 207214.CrossRefGoogle ScholarPubMed
Dong, K, Duan, HX, Liu, JT, Sun, L, Gu, SH, Yang, RN, Dhiloo, KH, Gao, XW, Zhang, YJ and Guo, Y-Y (2017b) Key site residues of pheromone-binding protein 1 involved in interacting with sex pheromone components of Helicoverpa armigera. Scientific Reports 7, 16859.CrossRefGoogle ScholarPubMed
Dong, XT, Liao, H, Zhu, GH, Khuhro, SA, Ye, ZF, Yan, Q and Dong, SL (2019) CRISPR/Cas9-mediated PBP1 and PBP3 mutagenesis induced significant reduction in electrophysiological response to sex pheromones in male Chilo suppressalis. Insect Sci. 26, 388399.CrossRefGoogle ScholarPubMed
Fang, N, Hu, Y, Mao, B, Bi, J, Zheng, Y, Guan, C, Wang, Y, Li, J, Mao, Y and Ai, H (2018) Molecular characterization and functional differentiation of three pheromone-binding proteins from Tryporyza intacta. Scientific Reports 8, 10774.CrossRefGoogle ScholarPubMed
Franco, TA, Xu, P, Brito, NF, Oliveira, DS, Wen, X, Moreira, MF, Unelius, CR, Leal, WS and Melo, ACA (2018) Reverse chemical ecology-based approach leading to the accidental discovery of repellents for Rhodnius prolixus, a vector of Chagas diseases refractory to DEET. Insect Biochemistry and Molecular Biology 103, 4652.CrossRefGoogle Scholar
Fu, X, Liu, Y, Li, Y, Ali, A and Wu, K (2014) Does Athetis lepigone moth (Lepidoptera: Noctuidae) take a long-distance migration? Journal of Economic Entomology 107, 9951002.CrossRefGoogle Scholar
Fu, XB, Zhang, YL, Qiu, YL, Song, XM, Wu, F, Feng, YL, Zhang, JY and Li, HL (2018) Physicochemical basis and comparison of two type II sex pheromone components binding with pheromone-binding protein 2 from tea geometrid, Ectropis obliqua. Journal of Agricultural and Food Chemistry 66, 1308413095.CrossRefGoogle ScholarPubMed
Gong, Y, Tang, H, Bohne, C and Plettner, E (2010) Binding conformation and kinetics of two pheromone-binding proteins from the Gypsy moth Lymantria dispar with biological and nonbiological ligands. Biochemistry 49, 793801.CrossRefGoogle ScholarPubMed
Grater, F, Xu, W, Leal, W and Grubmuller, H (2006) Pheromone discrimination by the pheromone-binding protein of Bombyx mori. Structure (London, England: 1993) 14, 15771586.CrossRefGoogle ScholarPubMed
Gu, SH, Zhou, JJ, Wang, GR, Zhang, YJ and Guo, YY (2013) Sex pheromone recognition and immunolocalization of three pheromone binding proteins in the black cutworm moth Agrotis ipsilon. Insect Biochemistry and Molecular Biology 43, 237251.CrossRefGoogle ScholarPubMed
Guo, H, Huang, LQ, Pelosi, P and Wang, CZ (2012) Three pheromone-binding proteins help segregation between two Helicoverpa species utilizing the same pheromone components. Insect Biochemistry and Molecular Biology 42, 708716.CrossRefGoogle ScholarPubMed
Hackett, SC and Bonsall, MB (2019) Insect pest control, approximate dynamic programming and the management of the evolution of resistance. Ecological Applications 29, e01851.CrossRefGoogle ScholarPubMed
Hanks, LM, Millar, JG, Mongold-Diers, JA, Wong, JCH, Meier, LR, Reagel, PF and Mitchell, RF (2012) Using blends of cerambycid beetle pheromones and host plant volatiles to simultaneously attract a diversity of cerambycid species. Canadian Journal of Forest Research 42, 10501059.CrossRefGoogle Scholar
Hansson, BS and Stensmyr, MC (2011) Evolution of insect olfaction. Neuron 72, 698711.CrossRefGoogle ScholarPubMed
Harrewijn, P, Minks, AK and Mollema, C (1994) Evolution of plant volatile production in insect-plant relationships. Chemoecology 5–6, 5573.CrossRefGoogle Scholar
Jiang, XF, Luo, LZ, Jiang, YY, Zhang, YJ, Zhang, L and Wang, ZY (2011) Damage characteristics and outbreak causes of Athetis lepigone in China. Plant Protection 37, 130133.Google Scholar
Jin, JY, Li, ZQ, Zhang, YN, Liu, NY and Dong, SL (2014) Different roles suggested by sex-biased expression and pheromone binding affinity among three pheromone binding proteins in the pink rice borer, Sesamia inferens (Walker) (Lepidoptera: Noctuidae). Journal of Insect Physiology 66, 7179.CrossRefGoogle ScholarPubMed
Ju, Q, Guo, XQ, Li, X, Jiang, XJ, Jiang, XG, Ni, WL and Qu, MJ (2017) Plant volatiles increase sex pheromone attraction of Holotrichia parallela (Coleoptera: Scarabaeoidea). Journal of Chemical Ecology 43, 236242.CrossRefGoogle ScholarPubMed
Kaissling, KE (2013) Kinetics of olfactory responses might largely depend on the odorant–receptor interaction and the odorant deactivation postulated for flux detectors. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 199, 879896.CrossRefGoogle ScholarPubMed
Karlson, P and Butenandt, A (1959) Pheromones (ectohormones) in insects. Annual Review of Entomology 4, 3958.CrossRefGoogle Scholar
Katti, S, Lokhande, N, Gonzalez, D, Cassill, A and Renthal, R (2013) Quantitative analysis of pheromone-binding protein specificity. Insect Molecular Biology 22, 3140.CrossRefGoogle ScholarPubMed
Kehat, M and Dunkelblum, E (1990) Behavioral response of male Heliothis armigera (Lepidoptera: Noctuidae) moths in a flight tunnel to combinations of components identified from female sex pheromone glands. Journal of Insect Behavior 3, 7583.CrossRefGoogle Scholar
Khuhro, SA, Liao, H, Dong, XT, Yu, Q, Yan, Q and Dong, SL (2017) Two general odorant binding proteins display high bindings to both host plant volatiles and sex pheromones in a pyralid moth Chilo suppressalis (Lepidoptera: Pyralidae). Journal of Asia-Pacific Entomology 20, 521528.CrossRefGoogle Scholar
Lassance, JM and Löfstedt, C (2013) Chemical communication: a jewel sheds light on signal evolution. Current Biology 23, R346R348.CrossRefGoogle ScholarPubMed
Laughlin, JD, Ha, TS, Jones, DNM and Smith, DP (2008) Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell 133, 12551265.CrossRefGoogle ScholarPubMed
Leal, WS, Barbosa, RM, 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
Lecomte, C, Pierre, D, Pouzat, J and Thibout, E (1998) Behavioural and olfactory variations in the leek moth, Acrolepiopsis assectella, after several generations of rearing under diverse conditions. Entomologia Experimentalis et Applicata 86, 305311.CrossRefGoogle Scholar
Lee, S, Lee, DW and Boo, KS (2005) Sex pheromone composition of the diamondback moth, Plutella xylostella(L) in Korea. Journal of Asia-Pacific Entomology 8, 243248.CrossRefGoogle Scholar
Li, QL, Yi, SC, Li, DZ, Nie, XP, Li, SQ, Wang, MQ and Zhou, AM (2018a) Optimization of reverse chemical ecology method: false positive binding of Aenasius bambawalei odorant binding protein 1 caused by uncertain binding mechanism. Insect Molecular Biology 27, 305318.CrossRefGoogle ScholarPubMed
Li, ZQ, Ma, L, Yin, Q, Cai, XM, Luo, ZX, Bian, L, Xin, ZJ, He, P and Chen, ZM (2018b) Gene identification of pheromone gland genes involved in type II sex pheromone biosynthesis and transportation in female tea pest Ectropis grisescens. G3 Genes|Genomes|Genetics 8, 899908.CrossRefGoogle ScholarPubMed
Li, CZ, Sun, H, Gao, Q, Bian, FY, Noman, A, Xiao, WH, Zhou, GX and Lou, YG (2020) Host plants alter their volatiles to help a solitary egg parasitoid distinguish habitats with parasitized hosts from those without. Plant Cell and Environment 43, 17401750.CrossRefGoogle Scholar
Linn, CEJ, Campbell, MGJ and Roelofs, WL (1987) Pheromone components and active spaces: what do moths smell and where do they smell it? Science (New York, N.Y.) 237, 650652.CrossRefGoogle Scholar
Liu, Z, Vidal, DM, Syed, VZ, Ishida, Y and Leal, WS (2010) Pheromone binding to general odorant-binding proteins from the navel orangeworm. Journal of Chemical Ecology 36, 787794.CrossRefGoogle ScholarPubMed
Liu, NY, Liu, CC and Dong, SL (2013) Functional differentiation of pheromone-binding proteins in the common cutworm Spodoptera litura. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 165, 254262.CrossRefGoogle ScholarPubMed
Liu, NY, Yang, F, Yang, K, He, P, Niu, XH, Xu, W, Anderson, A and Dong, SL (2015) Two subclasses of odorant-binding proteins in Spodoptera exigua display structural conservation and functional divergence. Insect Molecular Biology 24, 167182.CrossRefGoogle ScholarPubMed
Lo Pinto, M, Cangelosi, B and Colazza, S (2013) Female-released sex pheromones mediating courtship behavior in Lysiphlebus testaceipes males. Journal of Insect Science (Online) 13, 53.CrossRefGoogle ScholarPubMed
Lucas-Barbosa, D, Sun, P, Hakman, A, van Beek, TA, van Loon, JJA and Dicke, M (2015) Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Functional Ecology 30, 431441.CrossRefGoogle Scholar
Maffei, ME (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. South African Journal of Botany 76, 612631.CrossRefGoogle Scholar
Maïbèche-Coisné, M, Jacquin-Joly, E, François, MC and Meillour, PNL (1998) Molecular cloning of two pheromone binding proteins in the cabbage armyworm Mamestra brassicae. Insect Biochemistry and Molecular Biology 28, 815818.CrossRefGoogle ScholarPubMed
Maida, R, Krieger, J, Gebauer, T, Lange, U and Ziegelberger, G (2000) Three pheromone-binding proteins in olfactory sensilla of the two silkmoth species Antheraea polyphemus and Antheraea pernyi. European Journal of Biochemistry 267, 28992908.CrossRefGoogle ScholarPubMed
Maida, R, Ziegelberger, G and Kaissling, KE (2003) Ligand binding to six recombinant pheromone-binding proteins of Antheraea polyphemus and Antheraea pernyi. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 173, 565573.CrossRefGoogle ScholarPubMed
Matsuo, T, Sugaya, S, Yasukawa, J, Aigaki, T and Fuyama, Y (2007) Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biology 5, e118.CrossRefGoogle ScholarPubMed
Mazumder, S, Dahal, SR, Chaudhary, BP and Mohanty, S (2018) Structure and function studies of Asian Corn Borer Ostrinia furnacalis pheromone binding Protein2. Scientific Reports 8, 17105.CrossRefGoogle ScholarPubMed
Mondor, EB, Tremblay, MN, Awmack, CS and Lindroth, RL (2004) Divergent pheromone-mediated insect behaviour under global atmospheric change. Global Change Biology 10, 18201824.CrossRefGoogle Scholar
Morris, GM, Huey, R, Lindstrom, W, Sanner, MF, Belew, RK, Goodsell, DS and Olson, AJ (2009) Autodock4 and autodocktools4: automated docking with selective receptor flexibility. Journal of Computational Chemistry 30, 27852791.CrossRefGoogle ScholarPubMed
Ochieng, SA, Park, KC and Baker, TC (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 188, 325333.CrossRefGoogle ScholarPubMed
Odinokov, VN, Ishmuratov, GY, Ladenkova, IM, Sokol'skaya, OV, Muslukhov, RR, Akhmetova, VR and Tolstikov, GA (1993) Insect pheromones and their analogues XLVIII. A convenient synthesis of the 10E,12Z- and 10E,12E- isomers of hexadecadien-1-ol and of hexadeca-10E,12Z-dienal – components of the sex pheromone of the silkworm moth. Chemistry of Natural Compounds 29, 668673.CrossRefGoogle Scholar
Pelosi, P, Iovinella, I, Zhu, J, Wang, G and Dani, FR (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biological Reviews of the Cambridge Philosophical Society 93, 184200.CrossRefGoogle ScholarPubMed
Picimbon, JF and Gadenne, C (2002) Evolution of noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochemistry and Molecular Biology 32, 839846.CrossRefGoogle ScholarPubMed
Picimbon, JF, Gadenne, C, Bécard, JM, Clément, JL and Sreng, L (1997) Sex pheromone of the French black cutworm moth, Agrotis ipsilon (Lepidoptera: Noctuidae): identification and regulation of a multicomponent blend. Journal of Chemical Ecology 23, 211230.CrossRefGoogle Scholar
Purnamadjaja, AH and Russell, RA (2005) Pheromone communication in a robot swarm: necrophoric bee behaviour and its replication. Robotica 23, 731742.CrossRefGoogle Scholar
Renou, M and Anton, S (2020) Insect olfactory communication in a complex and changing world. Current Opinion in Insect Science 42, 17.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, 501518.CrossRefGoogle ScholarPubMed
Roelofs, WL, Comeau, A and Selle, R (1969) Sex pheromone of the oriental fruit moth. Nature 224, 723.CrossRefGoogle Scholar
Sarfraz, RM, Evenden, ML, Keddie, BA and Dosdall, LM (2005) Pheromone-mediated mating disruption: a powerful tool in insect pest management. 16, 4041.Google Scholar
Song, YQ, Sun, HZ and Du, J (2018) Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans Distant (Hemiptera: Lygaeidae). Scientific Reports 8, 7803.CrossRefGoogle ScholarPubMed
Soroka, JJ, Bartelt, RJ, Zilkowski, BW and Cosse, AA (2005) Responses of flea beetle Phyllotreta cruciferae to synthetic aggregation pheromone components and host plant volatiles in field trials. Journal of Chemical Ecology 31, 18291843.CrossRefGoogle ScholarPubMed
Sun, M, Liu, Y and Wang, G (2013) Expression patterns and binding properties of three pheromone binding proteins in the diamondback moth, Plutella xyllotella. Journal of Insect Physiology 59, 4655.CrossRefGoogle ScholarPubMed
Sweeney, J, De Groot, P, MacDonald, L, Smith, S, Cocquempot, C, Kenis, M and Gutowski, JM (2004) Host volatile attractants and traps for detection of Tetropium fuscum(F.),Tetropium castaneumL, and other longhorned beetles (Coleoptera: Cerambycidae). Environmental Entomology 33, 844854.CrossRefGoogle Scholar
Syed, Z, Ishida, Y, Taylor, K, Kimbrell, DA and Leal, WS (2006) Pheromone reception in fruit flies expressing a moth's odorant receptor. Proceedings of the National Academy of Sciences of the USA 103, 1653816543.CrossRefGoogle ScholarPubMed
Trott, O and Olson, AJ (2009) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry 31, 455461.Google Scholar
Tumlinson, JH, Mitchell, ER and Sonnet, PE (1981) Sex pheromone components of the beet armyworm, Spodoptera exigua. Journal of Environmental Science and Health, Part A 16, 189200.Google Scholar
Varela, N, Avilla, J, Anton, S and Gemeno, C (2011) Synergism of pheromone and host-plant volatile blends in the attraction of Grapholita molesta males. Entomologia Experimentalis et Applicata 141, 114122.CrossRefGoogle Scholar
Veire, M and Dirinck, P (1986) Sex pheromone components of the cabbage armyworm, Mamestra brassicae: isolation, identification and field experiments. Entomologia Experimentalis et Applicata 41, 153155.CrossRefGoogle Scholar
Venthur, H and Zhou, JJ (2018) Odorant receptors and odorant-binding proteins as insect pest control targets: a comparative analysis. Frontiers in Physiology 9, 1163.CrossRefGoogle ScholarPubMed
Verheggen, FJ, Arnaud, L, Bartram, S, Gohy, M and Haubruge, E (2008) Aphid and plant volatiles induce oviposition in an aphidophagous hoverfly. Journal of Chemical Ecology 34, 301307.CrossRefGoogle Scholar
Wang, H, Ma, YF, Wang, MM, Chen, GL, Dewer, Y, He, M, Zhang, F, Yang, YF, Liu, JF and He, P (2020) Expression, affinity, and functional characterization of the specific binding of two putative pheromone-binding proteins in the omnivorous German cockroach Blattella germanica. Journal of Agricultural and Food Chemistry 68, 1357313583.CrossRefGoogle ScholarPubMed
Xiu, WM, Zhou, YZ and Dong, SL (2008) Molecular characterization and expression pattern of two pheromone-binding proteins from Spodoptera litura (Fabricius). Journal of Chemical Ecology 34, 487498.CrossRefGoogle ScholarPubMed
Xu, H and Turlings, TCJ (2018) Plant volatiles as mate-finding cues for insects. Trends in Plant Science 23, 100111.CrossRefGoogle ScholarPubMed
Xu, P, Atkinson, R, Jones, DNM and Smith, DP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45, 193200.CrossRefGoogle ScholarPubMed
Yan, Q, Zheng, MY, Xu, JW, Ma, JF, Chen, Y, Dong, ZP, Liu, L, Dong, SL and Zhang, YN (2018) Female sex pheromone of Athetis lepigone (Lepidoptera: Noctuidae): identification and field evaluation. Journal of Applied Entomology 142, 125130.CrossRefGoogle Scholar
Yang, Z, Bengtsson, M and Witzgall, P (2004) Host plant volatiles synergize response to sex pheromone in codling moth, Cydia pomonella. Journal of Chemical Ecology 30, 619629.CrossRefGoogle ScholarPubMed
Yang, H, Su, T, Yang, W, Yang, CP, Chen, ZM, Lu, L, Liu, YL and Tao, YY (2017) Molecular characterization, expression pattern and ligand-binding properties of the pheromone-binding protein gene from Cyrtotrachelus buqueti. Physiological Entomology 42, 369378.CrossRefGoogle Scholar
Zhang, TT, Mei, XD, Feng, JN, Berg, BG, Zhang, YJ and Guo, YY (2012) Characterization of three pheromone-binding proteins (PBPs) of Helicoverpa armigera (Hubner) and their binding properties. Journal of Insect Physiology 58, 941948.CrossRefGoogle ScholarPubMed
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, 279286.CrossRefGoogle ScholarPubMed
Zhang, YN, Zhu, XY, Ma, JF, Dong, ZP, Xu, JW, Kang, K and Zhang, LW (2017) Molecular identification and expression patterns of odorant binding protein and chemosensory protein genes in Athetis lepigone (Lepidoptera: Noctuidae). PeerJ 5, e3157.CrossRefGoogle ScholarPubMed
Zhang, XQ, Yan, Q, Li, LL, Xu, JW, Mang, D, Wang, XL, Hoh, HH, Ye, J, Ju, Q, Ma, Y, Liang, M, Zhang, YY, Zhu, XY, Zhang, F, Dong, SL, Zhang, YN and Zhang, LW (2020a) Different binding properties of two general-odorant binding proteins in Athetis lepigone with sex pheromones, host plant volatiles and insecticides. Pesticide Biochemistry and Physiology 164, 173182.CrossRefGoogle ScholarPubMed
Zhang, YN, Xu, JW, Zhang, XC, Zhang, XQ, Li, LL, Yuan, X, Mang, DZ, Zhu, XY, Zhang, F, Dewer, Y, Xu, L and Wu, XM (2020b) Organophosphorus insecticide interacts with the pheromone-binding proteins of Athetis lepigone: implication for olfactory dysfunction. Journal of Hazardous Materials 397, 122777.CrossRefGoogle ScholarPubMed
Zhang, YN, Zhang, XQ, Zhang, XC, Xu, JW, Li, LL, Zhu, XY, Wang, JJ, Wei, JY, Mang, DZ, Zhang, F, Yuan, X and Wu, XM (2020c) Key amino acid residues influencing binding affinities of pheromone-binding protein from Athetis lepigone to two sex pheromones. Journal of Agricultural and Food Chemistry 68, 60926103.CrossRefGoogle ScholarPubMed
Zhou, JJ, Robertson, G, He, X, Dufour, S, Hooper, AM, Pickett, JA and Field, LM (2009) Characterisation of Bombyx mori odorant-binding proteins reveals that a general odorant-binding protein discriminates between sex pheromone components. Journal of Molecular Biology 389, 529545.CrossRefGoogle ScholarPubMed
Zhu, J, Ban, L, Song, LM, Liu, Y, Pelosi, P and Wang, G (2016) General odorant-binding proteins and sex pheromone guide larvae of Plutella xylostella to better food. Insect Biochemistry and Molecular Biology 72, 1019.CrossRefGoogle ScholarPubMed
Zhu, J, Arena, S, Spinelli, S, Liu, D, Zhang, G, Wei, R, Cambillau, C, Scaloni, A, Wang, G and Pelosi, P (2017) Reverse chemical ecology: olfactory proteins from the giant panda and their interactions with putative pheromones and bamboo volatiles. Proceedings of the National Academy of Sciences of the United States of America 114, E9802E9810.Google ScholarPubMed
Zhu, GH, Zheng, MY, Yan, Q, Sun, JB, Khuhro, SA, Huang, Y, Syed, Z and Dong, SL (2019) CRISPR/Cas9 mediated gene knockout reveals a more important role of PBP1 than PBP2 in the perception of female sex pheromone components in Spodoptera litura. Insect Biochemistry and Molecular Biology 115, 103244.CrossRefGoogle ScholarPubMed
Ziegelberger, G (1995) Redox-shift of the pheromone-binding protein in the silkmoth Antheraea polyphemus. European Journal of Biochemistry 232, 706711.CrossRefGoogle ScholarPubMed
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