The effects of plant volatiles on parasitoids are important with regards to the tri-trophic interactions among host plants, insect herbivores, and their natural enemies. However, the effects of plant volatiles on the important parasitoid (Microplitis pallidipes Szépligeti; Hymenoptera: Braconidae) of noctuids have not been determined at the molecular, laboratory, and outdoor scales with complementary approaches. The odorant binding protein 8 of M. pallidipes (MpOBP8) with an open reading frame of 459 bp was cloned and successfully expressed in Escherichia coli (Eubacteriales: Enterobacteriaceae). The purified protein MpOBP8 had a relatively high binding capacity to the plant volatile β-ionone (Ki value was 28.86 μM) in the fluorescence competitive binding assay. Meanwhile, Y-tube olfactometer experiments indicated that β-ionone selectively attracts the parasitic wasp as the ratio of M. pallidipes selecting β-ionone vs. control was 2:1. Likewise, field screenhouse experiments verified the above results as the ratio of M. pallidipes selecting β-ionone vs. control was close to 2:1. This study suggested that β-ionone is a plant volatile that attracts the parasitoid M. pallidipes, and MpOBP8 may play a key role in the discrimination of M. pallidipes in searching for hosts via β-ionone. In general our results suggest that β-ionone has the potential to enhance the biocontrol effect of parasitoids on insect herbivores.
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Abbas S, Perez-Hedo M, Colazza S, Urbaneja A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl 59:565–574
Armbruster P, White S, Dzundza J, Crawford J, Zhao XM (2009) Identification of genes encoding atypical odorant-binding proteins in Aedes albopictus (Diptera: Culicidae). J Med Entomol 46:271–280
Belz E, Kölliker M, Balmer O (2013) Olfactory attractiveness of flowering plants to the parasitoid Microplitis mediator: potential implications for biological control. BioControl 58:163–173
Beyaert I, Waschke N, Scholz A, Varama M, Reinecke A, Hilker M (2010) Relevance of resource-indicating key volatiles and habitat odour for insect orientation. Anim Behav 79:1077–1086
Cáceres LA, Lakshminarayan S, Yeung KC, Mcgarvey BD, Hannoufa A, Sumarah MW, Benitez X, Scott IM (2016) Repellent and attractive effects of α-, β-, and dihydro-β-ionone to generalist and specialist herbivores. J Chem Ecol 42:107–117
Calvello M, Brandazza A, Navarrini A, Danin FR, Turillazzi S, Felicioli A, Pelosi P (2005) Expression of odorant-binding proteins and chemosensory proteins in some Hymenoptera. Insect Biochem Molec 35:297–307
Cheng HC (2004) The influence of cooperativity on the determination of dissociation constants: examination of the Cheng-Prusoff equation, the Scatchard analysis, the Schild analysis and related power equations. Pharmacol Res 50:21–40
Cusumano A, Harvey JA, Dicke M, Poelman EH (2019) Hyperparasitoids exploit herbivore-induced plant volatiles during host location to assess host quality and non-host identity. Oecologia 189:699–709
Deem LS (2009) Behavioral responses of Diabroticite beetles to selected olfactory and visual cues (Coleoptera: Crysomelidae). PhD dissertation. University of Illinois at Urbana-Champaign, USA.
Farde L, Eriksson L, Blomquist G, Halldin C (1989) Kinetic analysis of central [11C] raclopride binding to D2-dopamine receptors studied by PET— a comparison to the equilibrium analysis. J Cerebr Blood F Met 9:696–708
Frago E, Mala M, Weldegergis BT, Yang C, Mclean A, Godfray HCJ, Gols R, Dicke M (2017) Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles. Nat Commun 8:1860
Gruber MY, Xu N, Grenkow L, Li X, Onyilagha J, Soroka JJ, Westcott ND, Hegedus DD (2009) Responses of the crucifer flea beetle to Brassica volatiles in an olfactometer. Environ Entomol 5:1467–1479
Hodge S, Ward JL, Galster AM, Beale MH, Powell G (2011) The effects of a plant defence priming compound, β-aminobutyric acid, on multitrophic interactions with an insect herbivore and a hymenopterous parasitoid. BioControl 56:699–711
Jiang JX, Yang JH, Ji XY, Zhang H, Wan NF (2018) Experimental temperature elevation promotes the cooperative ability of two natural enemies in the control of insect herbivores. Biol Control 117:52–62
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948
Li HW, Wang P, Zhang LW, Xu X, Cao ZW, Zhang L (2018) Expressions of olfactory proteins in locust olfactory organs and a palp odorant receptor involved in plant aldehydes detection. Front Physiol 9:664
Li KM, Wang SN, Zhang K, Ren L, Ali A, Zhang YJ, Zhou JJ, Guo YY (2014) Odorant binding characteristics of three recombinant odorant binding proteins in Microplitis mediator (Hymenoptera: Braconidae). J Chem Ecol 40:541–548
Liu NY, Zhu JY, Zhang T, Dong SL (2017) Characterization of two odorant binding proteins in Spodoptera exigua reveals functional conservation and difference. Comp Biochem Phys A 213:20–27
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Lundin O, Ward KL, Williams NM (2019) Identifying native plants for coordinated habitat management of arthropod pollinators, herbivores and natural enemies. J Appl Ecol 56:665–676
Magalhes DM, Da Silva ITFA, Borges M, Laumann RA, Blassioli-Moraes MC (2019) Anthonomus grandis aggregation pheromone induces cotton indirect defence and attracts the parasitic wasp Bracon vulgaris. J Exp Bot 70:1891–1901
Northey T, Venthur H, Biasio FD, Chauviac FX, Cole A, Junior KALR, Grossi G, Falabella P, Field LM, Keep NH, Zhou JJ (2016) Crystal structures and binding dynamics of odorant-binding protein 3 from two aphid species Megoura viciae and Nasonovia ribisnigri. Sci Rep 6:24739
Paparella A, Shaltiel-Harpaza L, Ibdah M (2021) β-ionone: its occurrence and biological function and metabolic engineering. Plants 10:754
Park KC, Zhu J, Harris J, Ochieng SA, Baker TC (2008) Electroantennogram responses of a parasitic wasp, Microplitis croceipes, to host-related volatile and anthropogenic compounds. Physiol Entomol 26:69–77
Paula DP, Togawa RC, Costa MMC, Grynberg P, Martins NF, Andow DA (2016) Identification and expression profile of odorant-binding proteins in Halyomorpha halys (Hemiptera: Pentatomidae). Insect Mol Biol 25:580–594
Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Sci 63:1658–1676
Ponzio C, Weldegergis BT, Dicke M, Gols R (2016) Compatible and incompatible pathogen–plant interactions differentially affect plant volatile emissions and the attraction of parasitoid wasps. Funct Ecol 30:1779–1789
Rabeschini G, Bergamo PJ, Nunes C (2021) Meaningful words in crowd noise: searching for volatiles relevant to carpenter bees among the diverse scent blends of bee flowers. J Chem Ecol 47:444–454
Rebijith KB, Asokan R, Hande HR, Kumar NKK, Krishna V, Vinutha J, Bakthacatsalam N (2015) RNA interference of odorant-binding protein 2 (OBP2) of the cotton aphid, Aphis gossypii (Glover), resulted in altered electrophysiological responses. Appl Biochem Biotech 178:251–266
Song YQ, Sun HZ, Du J (2018) Identification and tissue distribution of chemosensory protein and odorant binding protein genes in Tropidothorax elegans Distant (Hemiptera: Lygaeidae). Sci Rep 8:7803
Spinelli S, Lagarde A, Iovinella I, Legrand P, Tegoni M, Pelosi P, Cambillau C (2012) Crystal structure of Apis mellifera OBP14, a C-minus odorant-binding protein, and its complexes with odorant molecules. Insect Biochem Molec 42:41–50
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, DePaepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:0034.1-0034.11
Venthur H, Zhou JJ, Mutis A, Ceballos R, Mella-Herrera R, Larama G, Acila A, Iturriaga-Vasquez P, Faundez-Parraguez M, Alvear M, Quiroz A (2016) β-ionone as putative semiochemical suggested by ligand binding on an odorant-binding protein of Hylamorpha elegans and electroantennographic recordings. Entomol Sci 19:188–200
Wang SY, Gu SH, Han L, Guo YY, Zhang YJ (2013) Specific involvement of two amino acid residues in cis-nerolidol binding to odorant-binding protein 5 AlinOBP5 in the alfalfa plant bug, Adelphocoris lineolatus (goeze). Insect Mol Biol 22:172–182
Wu F, Huang JJ, Tan J, Tang MZ, Li HL (2016) Molecular cloning, prokaryotic expression and ligand-binding characterization of a novel pheromone binding protein OBP10 in Apis cerana cerana (Hymenoptera: Apidae). Acta Ent Sin 59:25–32
Young JM, Shykind BM, Lane RP, Tonnes-Priddy L, Ross JA, Walker M, Williams EM, Trask BJ (2003) Odorant receptor expressed sequence tags demonstrate olfactory expression of over 400 genes, extensive alternate splicing and unequal expression levels. Genome Biol 4:R71
Zhu XQ, Ding YX, Liu HW, Zhou YL, Zhang YJ, Guo YY (2015) Binding specificity analysis of odorant binding protein AlucOBP8 of Apolygus lucorum (Meyer-Dür). Chinese J Biol Control 31:821–829
This work was supported by the Shanghai Agriculture Applied Technology Development Program (Grant No. T20210204), National Natural Science Foundation of China (Grant No. 31601641, 32001969), Natural Science Foundation of Shanghai (Grant No. 20ZR1449000), Shanghai Agriculture Commission of China (2014-7-3-2) and SAAS Program for Excellent Research Team (2018[B-01]).
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Zhang, H., Wang, JY., Chen, YJ. et al. Beta-ionone is a functional plant volatile that attracts the parasitic wasp, Microplitis pallidipes. BioControl (2021). https://doi.org/10.1007/s10526-021-10117-3
- Biological control
- Field screenhouse experiments
- Fluorescence competitive binding assay
- Odorant binding protein
- Y-tube olfactometer