Abstract
Although synthetic pesticides are still used to control insect pests, greater efforts have been made to develop healthier and more environmentally friendly pesticides. Because of their insecticidal properties, botanical essential oils (EOs) are considered as promising alternatives to the use of synthetic insecticides. However, little is known about mechanisms underlying the insecticidal activity of most these natural compounds. In the present study, we evaluated the contact toxicity and the modes of action of the EO from Mentha arvensis against the granary weevil, Sitophilus granarius L. (Coleoptera: Curculionidae), a cosmopolitan insect pest that causes extensive damage to stored cereals. M. arvensis EO caused high contact toxicity in S. granarius adults, resulting in a rapid paralysis and rapid alteration of walking behavior. Our label-free quantitative proteomics approach revealed that M. arvensis EO induced dramatic physiological changes in exposed insects. The majority of the differentially expressed proteins (DEPs) were upregulated and are related to the development and functioning of the muscular and nervous systems, cellular respiration, protein synthesis, and detoxification. These results suggest that M. arvensis essential oil is capable of affecting a variety of biological processes, and shed light on the repair mechanisms put in place in surviving insects to counter the damage inflicted. This work opens new perspectives on the proposed mechanisms of insecticidal activity of a promising EO for controlling pests of stored cereals and may represent a first step in the development of novel bio-rational insecticides.
Similar content being viewed by others
Code availability
The python code used for video tracking is publicly available from the following link: https://gitlab.com/abaoula/codes-opencv
References
Abraham DM, Wolf MJ (2013) Disruption of sarcoendoplasmic reticulum calcium ATPase function in Drosophila leads to cardiac dysfunction. PLoS ONE 8:e77785. https://doi.org/10.1371/journal.pone.0077785
Aggarwal KK, Tripathi AK, Ahmad A et al (2001) Toxicity of l-menthol and its derivatives against four storage insects. Int J Trop Insect Sci 21:229–235. https://doi.org/10.1017/S1742758400007621
Andersen SO (2012) 6-Cuticular sclerotization and tanning. In: Gilbert LI (ed) Insect Molecular Biology and Biochemistry. Academic Press, San Diego, pp 167–192
Ansari MA, Vasudevan P, Tandon M, Razdan RK (2000) Larvicidal and mosquito repellent action of peppermint (Mentha piperita) oil. Bioresour Technol 71:267–271. https://doi.org/10.1016/S0960-8524(99)00079-6
Balabanidou V, Grigoraki L, Vontas J (2018) Insect cuticle: a critical determinant of insecticide resistance. Curr Opin Insect Sci 27:68–74. https://doi.org/10.1016/j.cois.2018.03.001
Banerjee S, Joshi R, Venkiteswaran G et al (2006) Compensation of Inositol 1,4,5-Trisphosphate receptor function by altering Sarco-Endoplasmic reticulum calcium ATPase activity in the Drosophila flight circuit. J Neurosci 26:8278–8288. https://doi.org/10.1523/JNEUROSCI.1231-06.2006
Bataillé L, Delon I, Da Ponte JP et al (2010) Downstream of identity genes: muscle-type-specific regulation of the fusion process. Dev Cell 19:317–328. https://doi.org/10.1016/j.devcel.2010.07.008
Benna C, Peron S, Rizzo G et al (2009) Post-transcriptional silencing of the Drosophila homolog of human ZASP: a molecular and functional analysis. Cell Tissue Res 337:463–476. https://doi.org/10.1007/s00441-009-0813-y
Bi J, Wang W, Liu Z et al (2014) Seipin promotes adipose tissue fat storage through the ER Ca2+-ATPase SERCA. Cell Metab 19:861–871. https://doi.org/10.1016/j.cmet.2014.03.028
Biswas NN, Saha S, Ali MK (2014) Antioxidant, antimicrobial, cytotoxic and analgesic activities of ethanolic extract of Mentha arvensis L. Asian Pac J Trop Biomed 4:792–797. https://doi.org/10.12980/APJTB.4.2014C1298
Bloomquist JR (2003) Chloride channels as tools for developing selective insecticides. Arch Insect Biochem Physiol 54:145–156. https://doi.org/10.1002/arch.10112
Bonner JM, Boulianne GL (2017) Diverse structures, functions and uses of FK506 binding proteins. Cell Signal 38:97–105. https://doi.org/10.1016/j.cellsig.2017.06.013
Bredendiek N, Hütte J, Steingräber A et al (2011) Go α is involved in sugar perception in Drosophila. Chem Senses 36:69–81. https://doi.org/10.1093/chemse/bjq100
Bronk P, Wenniger JJ, Dawson-Scully K et al (2001) Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron 30:475–488. https://doi.org/10.1016/S0896-6273(01)00292-6
Brügger BP, Martínez LC, Plata-Rueda A et al (2019) Bioactivity of the Cymbopogon citratus (Poaceae) essential oil and its terpenoid constituents on the predatory bug, Podisus nigrispinus (Heteroptera: Pentatomidae). Sci Rep 9:8358. https://doi.org/10.1038/s41598-019-44709-y
Cao T, Sujkowski A, Cobb T et al (2020) The glutamic acid-rich long C-terminal extension of troponin T has a critical role in insect muscle functions. J Biol Chem JBC.RA119.012014. https://doi.org/10.1074/jbc.RA119.012014
Cetin H, Cinbilgel I, Yanikoglu A, Gokceoglu M (2006) Larvicidal activity of some labiatae (lamiaceae) plant extracts from Turkey. Phytother Res 20:1088–1090. https://doi.org/10.1002/ptr.2004
Cetin H, Yanikoglu A (2006) A study of the larvicidal activity of Origanum (Labiatae) species from southwest Turkey. J Vector Ecol J Soc Vector Ecol 31:118–122. https://doi.org/10.3376/1081-1710(2006)31[118:asotla]2.0.co;2
Chen NH, Djoko KY, Veyrier FJ, McEwan AG (2016) Formaldehyde stress responses in bacterial pathogens. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00257
Cheng MY, Hartl FU, Martin J et al (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337:620–625. https://doi.org/10.1038/337620a0
Clark KA, Bland JM, Beckerle MC (2007) The Drosophila muscle LIM protein, Mlp84B, cooperates with D-titin to maintain muscle structural integrity. J Cell Sci 120:2066–2077. https://doi.org/10.1242/jcs.000695
Coats JR, Karr LL, Drewes CD (1991) Toxicity and neurotoxic effects of monoterpenoids. In: Naturally occurring pest bioregulators. American Chemical Society, pp 305–316
Copping LG, Menn JJ (2000) Biopesticides: a review of their action, applications and efficacy. Pest Manag Sci 56:651–676. https://doi.org/10.1002/1526-4998(200008)56:8%3c651::AID-PS201%3e3.0.CO;2-U
Dale C (2017) Evolution: Weevils get tough on symbiotic tyrosine. Curr Biol 27:R1282–R1284. https://doi.org/10.1016/j.cub.2017.10.031
Decoville M, Giacomello E, Leng M, Locker D (2001) DSP1, an HMG-like protein, is involved in the regulation of homeotic genes. Genetics 157:237–244
Deletre E, Chandre F, Barkman B et al (2016) Naturally occurring bioactive compounds from four repellent essential oils against Bemisia tabaci whiteflies: Bioactive natural repellent compounds against whiteflies. Pest Manag Sci 72:179–189. https://doi.org/10.1002/ps.3987
Demeter S, Lebbe O, Hecq F et al (2021) Insecticidal activity of 25 essential oils on the stored product pest. Sitophilus granarius Foods 10:200. https://doi.org/10.3390/foods10020200
Dick T, Ray K, Salz HK, Chia W (1996) Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol Cell Biol 16:1966–1977
Domingo A, González-Jurado J, Maroto M et al (1998) Troponin-T is a calcium-binding protein in insect muscle: in vivo phosphorylation, muscle-specific isoforms and developmental profile in Drosophila melanogaster. J Muscle Res Cell Motil 19:393–403. https://doi.org/10.1023/a:1005349704790
Echard A, Hickson GRX, Foley E, O’Farrell PH (2004) Terminal cytokinesis events uncovered after an RNAi screen. Curr Biol CB 14:1685–1693. https://doi.org/10.1016/j.cub.2004.08.063
Enan E (2001) Insecticidal activity of essential oils: octopaminergic sites of action. Comp Biochem Physiol Part C Toxicol Pharmacol 130:325–337. https://doi.org/10.1016/S1532-0456(01)00255-1
Enan EE (2005) Molecular and pharmacological analysis of an octopamine receptor from American cockroach and fruit fly in response to plant essential oils. Arch Insect Biochem Physiol 59:161–171. https://doi.org/10.1002/arch.20076
Featherstone DE, Rushton E, Broadie K (2002) Developmental regulation of glutamate receptor field size by nonvesicular glutamate release. Nat Neurosci 5:141–146. https://doi.org/10.1038/nn789
Fontanesi F, Soto IC, Barrientos A (2008) Cytochrome c oxidase biogenesis: new levels of regulation. IUBMB Life 60:557–568. https://doi.org/10.1002/iub.86
Ghosh-Roy A, Desai BS, Ray K (2005) Dynein light chain 1 regulates dynamin-mediated F-Actin assembly during sperm individualization in Drosophila. Mol Biol Cell 16:3107–3116. https://doi.org/10.1091/mbc.e05-02-0103
Gil A, de la Fuente EB, Lenardis AE et al (2002) Coriander essential oil composition from two genotypes grown in different environmental conditions J Agric Food Chem 50:2870–2877. https://doi.org/10.1021/jf011128i
Gonzalez CF, Proudfoot M, Brown G et al (2006) Molecular basis of formaldehyde detoxification characterization of two S-formylgluthione hydrolases from Escherichia coli, FrmB and YeiG. J Biol Chem 281:14514–14522. https://doi.org/10.1074/jbc.M600996200
Govindarajan M, Sivakumar R, Rajeswari M, Yogalakshmi K (2012) Chemical composition and larvicidal activity of essential oil from Mentha spicata (Linn.) against three mosquito species. Parasitol Res 110:2023–2032. https://doi.org/10.1007/s00436-011-2731-7
Guedes RNC, Lima JOG, Santos JP, Cruz CD (1994) Inheritance of Deltamethrin resistance in a Brazilian strain of maize weevil (Sitophilus zeamais mots.). Int J Pest Manag 40:103–106. https://doi.org/10.1080/09670879409371863
Handford CE, Elliott CT, Campbell K (2015) A review of the global pesticide legislation and the scale of challenge in reaching the global harmonization of food safety standards. Integr Environ Assess Manag 11:525–536. https://doi.org/10.1002/ieam.1635
Herold N, Will CL, Wolf E et al (2009) Conservation of the Protein Composition and Electron Microscopy Structure of Drosophila melanogaster and Human Spliceosomal Complexes. Mol Cell Biol 29:281–301. https://doi.org/10.1128/MCB.01415-08
Hirota B, Okude G, Anbutsu H et al (2017) A novel, extremely elongated, and endocellular bacterial symbiont supports cuticle formation of a grain pest beetle. mBio 8:e01482–17. https://doi.org/10.1128/mBio.01482-17
Horváth P, Koščová J (2017) In vitro antibacterial activity of Mentha essential oils against Staphylococcus aureus. Folia Vet 61:71–77. https://doi.org/10.1515/fv-2017-0030
Huang Y, Liao M, Yang Q et al (2019) iTRAQ-based quantitative proteome revealed metabolic changes of Sitophilus zeamais in response to terpinen-4-ol fumigation. Pest Manag Sci 75:444–451. https://doi.org/10.1002/ps.5135
Isman MB (2000) Plant essential oils for pest and disease management. Crop Prot 19:603–608. https://doi.org/10.1016/S0261-2194(00)00079-X
Isman MB, Grieneisen ML (2014) Botanical insecticide research: many publications, limited useful data. Trends Plant Sci 19:140–145. https://doi.org/10.1016/j.tplants.2013.11.005
Jan Y-N, Jan LY (2010) Branching out: mechanisms of dendritic arborization. Nat Rev Neurosci 11:316–328. https://doi.org/10.1038/nrn2836
Jankowska M, Rogalska J, Wyszkowska J, Stankiewicz M (2018) Molecular targets for components of essential oils in the insect nervous system—a review. Molecules 23:34. https://doi.org/10.3390/molecules23010034
Jayaram SA, Senti K-A, Tiklová K et al (2008) COPI vesicle transport is a common requirement for tube expansion in Drosophila. PLoS ONE 3:e1964. https://doi.org/10.1371/journal.pone.0001964
Jayas DS, White NDG, Muir WE (1994) Stored-grain ecosystems. CRC Press, Boca Raton
Jembere B, Obeng-Ofori D, Hassanali A, Nyamasyo GNN (1995) Products derived from the leaves of Ocimum kilimandscharicum (Labiatae) as post-harvest grain protectants against the infestation of three major stored product insect pests. Bull Entomol Res 85:361–367. https://doi.org/10.1017/S0007485300036099
Keeling CI, Yuen MM, Liao NY et al (2013) Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol 14:R27. https://doi.org/10.1186/gb-2013-14-3-r27
Kim S-I, Roh J-Y, Kim D-H et al (2003) Insecticidal activities of aromatic plant extracts and essential oils against Sitophilus oryzae and Callosobruchus chinensis. J Stored Prod Res 39:293–303. https://doi.org/10.1016/S0022-474X(02)00017-6
Klingenberg M (1985) The ADP/ATP carrier in mitochondrial membranes. In: Martonosi AN (ed) The enzymes of biological membranes, vol 4. Bioenergetics of Electron and Proton Transport. Springer, US, Boston, MA, pp 511–553
Kljajić P, Perić I (2007) Altered susceptibility of granary weevil Sitophilus granarius (L.) (Coleoptera: Curculionidae) populations to insecticides after selection with pirimiphos-methyl and deltamethrin. J Stored Prod Res 43:134–141. https://doi.org/10.1016/j.jspr.2006.02.004
Klymenko T, Papp B, Fischle W et al (2006) A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities. Genes Dev 20:1110–1122. https://doi.org/10.1101/gad.377406
Koliopoulos G, Pitarokili D, Kioulos E et al (2010) Chemical composition and larvicidal evaluation of Mentha, Salvia, and Melissa essential oils against the West Nile virus mosquito Culex pipiens. Parasitol Res 107:327–335. https://doi.org/10.1007/s00436-010-1865-3
Koon AC, Budnik V (2012) Inhibitory control of synaptic and behavioral plasticity by octopaminergic signaling. J Neurosci 32:6312–6322. https://doi.org/10.1523/JNEUROSCI.6517-11.2012
Kostyukovsky M, Rafaeli A, Gileadi C et al (2002) Activation of octopaminergic receptors by essential oil constituents isolated from aromatic plants: possible mode of action against insect pests. Pest Manag Sci 58:1101–1106. https://doi.org/10.1002/ps.548
Kumar A, Shukla R, Singh P et al (2009) Use of essential oil from Mentha arvensis L. to control storage moulds and insects in stored chickpea. J Sci Food Agric 89:2643–2649. https://doi.org/10.1002/jsfa.3768
Kumar P, Mishra S, Malik A, Satya S (2011) Insecticidal properties of Mentha species: a review. Ind Crops Prod 34:802–817. https://doi.org/10.1016/j.indcrop.2011.02.019
Kumar R, Dubey NK, Tiwari OP et al (2007) Evaluation of some essential oils as botanical fungitoxicants for the protection of stored food commodities from fungal infestation. J Sci Food Agric 87:1737–1742. https://doi.org/10.1002/jsfa.2906
Lee B-H, Choi W-S, Lee S-E, Park B-S (2001) Fumigant toxicity of essential oils and their constituent compounds towards the rice weevil, Sitophilus oryzae (L.). Crop Prot 20:317–320. https://doi.org/10.1016/S0261-2194(00)00158-7
Leroux MR, Hartl FU (2000) Protein folding: versatility of the cytosolic chaperonin TRiC/CCT. Curr Biol 10:R260–R264. https://doi.org/10.1016/S0960-9822(00)00432-2
Li S-G, Li M-Y, Huang Y-Z et al (2013) Fumigant activity of Illicium verum fruit extracts and their effects on the acetylcholinesterase and glutathione S-transferase activities in adult Sitophilus zeamais. J Pest Sci 86:677–683. https://doi.org/10.1007/s10340-013-0520-z
Li W, Gao F-B (2003) Actin filament-stabilizing protein tropomyosin regulates the size of dendritic fields. J Neurosci Off J Soc Neurosci 23:6171–6175
Li W, Ye Y (2008) Polyubiquitin chains: functions, structures, and mechanisms. Cell Mol Life Sci CMLS 65:2397–2406. https://doi.org/10.1007/s00018-008-8090-6
Liao M, Xiao J-J, Zhou L-J et al (2016) Insecticidal activity of Melaleuca alternifolia essential oil and RNA-Seq analysis of Sitophilus zeamais transcriptome in response to oil fumigation. PLoS ONE 11:e0167748. https://doi.org/10.1371/journal.pone.0167748
Liao M, Yang Q-Q, Xiao J-J et al (2018) Toxicity of Melaleuca alternifolia essential oil to the mitochondrion and NAD+/NADH dehydrogenase in Tribolium confusum. PeerJ 6:e5693. https://doi.org/10.7717/peerj.5693
Likhoshvai V, Ratushny A (2007) Generalized hill function method for modeling molecular processes. J Bioinform Comput Biol 05:521–531. https://doi.org/10.1142/S0219720007002837
López MD, Pascual-Villalobos MJ (2010) Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Ind Crops Prod 31:284–288. https://doi.org/10.1016/j.indcrop.2009.11.005
Ložienė K, Venskutonis PR (2005) Influence of environmental and genetic factors on the stability of essential oil composition of Thymus pulegioides. Biochem Syst Ecol 33:517–525. https://doi.org/10.1016/j.bse.2004.10.004
Magan N, Hope R, Cairns V, Aldred D (2003) Post-harvest fungal ecology: Impact of fungal growth and mycotoxin accumulation in stored grain. In: Xu X, Bailey JA, Cooke BM (eds) Epidemiology of Mycotoxin Producing Fungi: Under the aegis of COST Action 835 ‘Agriculturally Important Toxigenic Fungi 1998–2003’, EU project (QLK 1-CT-1998–01380). Springer, Netherlands, Dordrecht, pp 723–730
Mansour EE, Mi F, Zhang G et al (2012) Effect of allylisothiocyanate on Sitophilus oryzae, Tribolium confusum and Plodia interpunctella: Toxicity and effect on insect mitochondria. Crop Prot 33:40–51. https://doi.org/10.1016/j.cropro.2011.11.010
Mishra BB, Tripathi SP, Tripathi CPM (2012) Response of Tribolium castaneum (Coleoptera: Tenebrionidae) and Sitophilus oryzae (Coleoptera: Curculionidae) to potential insecticide derived from essential oil of Mentha arvensis leaves. Biol Agric Hortic 28:34–40. https://doi.org/10.1080/01448765.2012.662792
Miyazawa M, Watanabe H, Kameoka H (1997) Inhibition of Acetylcholinesterase activity by Monoterpenoids with a p-Menthane skeleton. J Agric Food Chem 45:677–679. https://doi.org/10.1021/jf960398b
Moraru A, Cakan-Akdogan G, Strassburger K et al (2017) THADA regulates the organismal balance between energy storage and heat production. Dev Cell 41:72-81.e6. https://doi.org/10.1016/j.devcel.2017.03.016
Mosrin-Huaman C, Canaple L, Locker D, Decoville M (1998) DSP1 gene of Drosophila melanogaster encodes an HMG-domain protein that plays multiple roles in development. Dev Genet 23:324–334. https://doi.org/10.1002/(SICI)1520-6408(1998)23:4%3c324::AID-DVG7%3e3.0.CO;2-T
Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101:372–378. https://doi.org/10.1016/j.biortech.2009.07.048
Ngamo L, Hance T (2007) Diversité des ravageurs des denrée et méthodes alternatives de lutte en milieu tropical. Tropicultura 25
Noh MY, Kramer KJ, Muthukrishnan S et al (2015) Loss of function of the yellow-e gene causes dehydration-induced mortality of adult Tribolium castaneum. Dev Biol 399:315–324. https://doi.org/10.1016/j.ydbio.2015.01.009
Norden DA, Matanganyidze C (1979) Activities of kreb’s cycle enzymes in the flight muscles of the tsetse fly (Glossina) and the fleshfly (Sarcophaga). Insect Biochem 9:85–87. https://doi.org/10.1016/0020-1790(79)90030-1
Noudjou F, Kouninki H, Ngamo LST et al (2007) Effect of site location and collecting period on the chemical composition of Hyptis Spicigera Lam. an insecticidal essential oil from North-Cameroon. J Essent Oil Res 19:597–601. https://doi.org/10.1080/10412905.2007.9699340
O’Connor-Giles KM, Ho LL, Ganetzky B (2008) Nervous Wreck interacts with Thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58:507–518. https://doi.org/10.1016/j.neuron.2008.03.007
Ohler S, Hakeda-Suzuki S, Suzuki T (2011) Hts, the Drosophila homologue of Adducin, physically interacts with the transmembrane receptor Golden goal to guide photoreceptor axons. Dev Dyn Off Publ Am Assoc Anat 240:135–148. https://doi.org/10.1002/dvdy.22515
Olesnicky EC, Wright EG (2018) Drosophila as a model for assessing the function of RNA-binding proteins during neurogenesis and neurological disease. J Dev Biol 6. https://doi.org/10.3390/jdb6030021
Oliveira AP, Santana AS, Santana EDR et al (2017) Nanoformulation prototype of the essential oil of Lippia sidoides and thymol to population management of Sitophilus zeamais (Coleoptera: Curculionidae). Ind Crops Prod 107:198–205. https://doi.org/10.1016/j.indcrop.2017.05.046
Oliveira AP, Santos AA, Santana AS et al (2018) Essential oil of Lippia sidoides and its major compound thymol: Toxicity and walking response of populations of Sitophilus zeamais (Coleoptera: Curculionidae). Crop Prot 112:33–38. https://doi.org/10.1016/j.cropro.2018.05.011
Olivero-Verbel J, Nerio LS, Stashenko EE (2010) Bioactivity against Tribolium castaneum Herbst (Coleoptera: Tenebrionidae) of Cymbopogon citratus and Eucalyptus citriodora essential oils grown in Colombia. Pest Manag Sci 66:664–668. https://doi.org/10.1002/ps.1927
Omkar (2018) Pests and their management. Springer, Heidelberg
Pavela R, Benelli G (2016) Essential oils as Ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21:1000–1007. https://doi.org/10.1016/j.tplants.2016.10.005
Peña C, Hurt E, Panse VG (2017) Eukaryotic ribosome assembly, transport and quality control. Nat Struct Mol Biol 24:689–699. https://doi.org/10.1038/nsmb.3454
Plata-Rueda A, Campos JM, da Silva RG et al (2018) Terpenoid constituents of cinnamon and clove essential oils cause toxic effects and behavior repellency response on granary weevil, Sitophilus granarius. Ecotoxicol Environ Saf 156:263–270. https://doi.org/10.1016/j.ecoenv.2018.03.033
Pokrywka NJ, Zhang H, Raley-Susman K (2014) Distinct roles for hu li tai shao and swallow in cytoskeletal organization during Drosophila oogenesis. Dev Dyn Off Publ Am Assoc Anat 243:906–916. https://doi.org/10.1002/dvdy.24132
Popović Z, Kostić M, Popović S, Skorić S (2006) Bioactivities of essential oils from Basil and Sage to Sitophilus Oryzae L. Biotechnol Biotechnol Equip 20:36–40. https://doi.org/10.1080/13102818.2006.10817301
Pourya M, Sadeghi A, Ghobari H et al (2018) Bioactivity of Pistacia atlantica desf. Subsp. Kurdica (Zohary) Rech. F. and Pistacia khinjuk stocks essential oils against Callosobruchus maculatus (F, 1775) (Coloeptera: Bruchidae) under laboratory conditions. J Stored Prod Res 77:96–105. https://doi.org/10.1016/j.jspr.2018.03.007
Preall JB, Czech B, Guzzardo PM et al (2012) shutdown is a component of the Drosophila piRNA biogenesis machinery. RNA 18:1446–1457. https://doi.org/10.1261/rna.034405.112
Rafti F, Scarvelis D, Lasko PF (1996) A Drosophila melanogaster homologue of the human DEAD-box gene DDX1. Gene 171:225–229. https://doi.org/10.1016/0378-1119(96)00034-0
Rattan RS (2010) Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Prot 29:913–920. https://doi.org/10.1016/j.cropro.2010.05.008
Regev U, Shalit H, Gutierrez AP (1983) On the optimal allocation of pesticides with increasing resistance: the case of alfalfa weevil. J Environ Econ Manag 10:86–100. https://doi.org/10.1016/0095-0696(83)90017-7
Regnault-Roger C, Vincent C, Arnason JT (2012) Essential oils in insect control: low-risk products in a high-Stakes World. Annu Rev Entomol 57:405–424. https://doi.org/10.1146/annurev-ento-120710-100554
Rodal AA, Motola-Barnes RN, Littleton JT (2008) Nervous Wreck and Cdc42 Cooperate to regulate endocytic Actin assembly during synaptic growth. J Neurosci 28:8316–8325. https://doi.org/10.1523/JNEUROSCI.2304-08.2008
Sanyal S, Consoulas C, Kuromi H et al (2005) Analysis of conditional paralytic mutants in Drosophila sarco-endoplasmic reticulum calcium ATPase reveals novel mechanisms for regulating membrane excitability. Genetics 169:737–750. https://doi.org/10.1534/genetics.104.031930
Saroukolai AT, Moharramipour S, Meshkatalsadat MH (2010) Insecticidal properties of Thymus persicus essential oil against Tribolium castaneum and Sitophilus oryzae. J Pest Sci 83:3–8. https://doi.org/10.1007/s10340-009-0261-1
Sasikumar AN, Perez WB, Kinzy TG (2012) The many roles of the eukaryotic elongation factor 1 complex. Wiley Interdiscip Rev RNA 3:543–555. https://doi.org/10.1002/wrna.1118
Schaneberg BT, Khan IA (2002) Comparison of extraction methods for marker compounds in the essential oil of Lemon Grass by GC. J Agric Food Chem 50:1345–1349. https://doi.org/10.1021/jf011078h
Schmucker D, Jackle H, Gaul U (1997) Genetic analysis of the larval optic nerve projection in Drosophila. Development 124:937–948
Schnorrer F, Schönbauer C, Langer CCH et al (2010) Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464:287–291. https://doi.org/10.1038/nature08799
Storey CL, Sauer DB, Walker D (1984) Present use of pest management practices in wheat, corn, and oats stored on the farm. J Econ Entomol 77:784–788. https://doi.org/10.1093/jee/77.3.784
Suh GSB, Poeck B, Chouard T et al (2002) Drosophila JAB1/CSN5 Acts in Photoreceptor Cells to Induce Glial Cells. Neuron 33:35–46. https://doi.org/10.1016/S0896-6273(01)00576-1
Tak J-H, Jovel E, Isman MB (2017) Effects of rosemary, thyme and lemongrass oils and their major constituents on detoxifying enzyme activity and insecticidal activity in Trichoplusia ni. Pestic Biochem Physiol 140:9–16. https://doi.org/10.1016/j.pestbp.2017.01.012
Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28. https://doi.org/10.1093/nar/29.1.22
Tetzlaff MT, Jäckle H, Pankratz MJ (1996) Lack of Drosophila cytoskeletal tropomyosin affects head morphogenesis and the accumulation of oskar mRNA required for germ cell formation. EMBO J 15:1247–1254. https://doi.org/10.1002/j.1460-2075.1996.tb00466.x
Thorpe C, Kim JJ (1995) Structure and mechanism of action of the acyl-CoA dehydrogenases. FASEB J 9:718–725. https://doi.org/10.1096/fasebj.9.9.7601336
Tiwari P (2016) Recent advances and challenges in trichome research and essential oil biosynthesis in Mentha arvensis L. Ind Crops Prod 82:141–148. https://doi.org/10.1016/j.indcrop.2015.11.069
Tripathi AK (2018) Pests of stored grains. In: Omkar (ed) Pests and their management. Springer Singapore, Singapore, pp 311–359
Tripathi AK, Prajapati V, Aggarwal KK, Kumar S (2000) Effect of volatile oil constituents of Mentha species against the stored grain pests, Callosobruchus maculatus and Tribolium castaneum. J Med Aromat Plant Sci 22:549–556
True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647. https://doi.org/10.1016/j.tree.2003.09.006
Varma J, Dubey NK (2001) Efficacy of essential oils of Caesulia axillaris and Mentha arvensis against some storage pests causing biodeterioration of food commodities. Int J Food Microbiol 68:207–210. https://doi.org/10.1016/S0168-1605(01)00506-2
Vigneron A, Masson F, Vallier A et al (2014) Insects recycle endosymbionts when the benefit is over. Curr Biol 24:2267–2273. https://doi.org/10.1016/j.cub.2014.07.065
Wan P-J, Fu K-Y, Lü F-G et al (2015) Knockdown of a putative alanine aminotransferase gene affects amino acid content and flight capacity in the Colorado potato beetle Leptinotarsa decemlineata. Amino Acids 47:1445–1454. https://doi.org/10.1007/s00726-015-1978-1
Wei N, Deng XW (2003) The COP9 signalosome. Annu Rev Cell Dev Biol 19:261–286. https://doi.org/10.1146/annurev.cellbio.19.111301.112449
Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141–143. https://doi.org/10.1016/0003-2697(84)90782-6
Wittkopp PJ, True JR, Carroll SB (2002) Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Dev Camb Engl 129:1849–1858
Yi P, Johnson AN, Han Z et al (2008) Heterotrimeric G proteins regulate a noncanonical function of septate junction proteins to maintain cardiac integrity in Drosophila. Dev Cell 15:704–713. https://doi.org/10.1016/j.devcel.2008.10.001
Zhang D, Marlin MC, Liang Z et al (2016) The Protein Tyrosine Phosphatase MEG2 Regulates the Transport and Signal Transduction of Tropomyosin Receptor Kinase A. J Biol Chem 291:23895–23905. https://doi.org/10.1074/jbc.M116.728550
Zhang J, Li D, Ge P et al (2013) RNA interference revealed the roles of two carboxylesterase genes in insecticide detoxification in Locusta migratoria. Chemosphere 93:1207–1215. https://doi.org/10.1016/j.chemosphere.2013.06.081
Zhao HW, Zhou D, Nizet V, Haddad GG (2010) Experimental selection for Drosophila survival in extremely high O2 environments. PLoS ONE 5:e11701. https://doi.org/10.1371/journal.pone.0011701
Zhou Y, Wang Y, Schreader BA, Nambu JR (2013) Drosophila Morgue associates with SkpA and Polyubiquitin in vivo. PLoS ONE 8:e74860. https://doi.org/10.1371/journal.pone.0074860
Zot AS, Potter JD (1987) Structural aspects of Troponin-Tropomyosin regulation of skeletal muscle contraction. Annu Rev Biophys Biophys Chem 16:535–559. https://doi.org/10.1146/annurev.bb.16.060187.002535
Acknowledgements
We would like to thank the ERASMUS + EOHUB project which aims to disseminate knowledge in the field of essential oils, as well as the Education, Audio-visual and Culture Executive Agency (EACEA) through the EOHUB project 600873-EPP1-2018-1ES-EPPKA2-KA. Thanks to Saskia Sergeant for her technical assistance. We are grateful to Guillaume Le Goff for his comments. This is publication BRC 269 of the Biodiversity Research Centre at UCLouvain.
Funding
This research was supported by the WALInnove program of the Walloon Region (Belgium) under the convention no1610128, Oilprotect project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Communicated by Murray Isman.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file4 (MP4 35486 kb)
Rights and permissions
About this article
Cite this article
Renoz, F., Demeter, S., Degand, H. et al. The modes of action of Mentha arvensis essential oil on the granary weevil Sitophilus granarius revealed by a label-free quantitative proteomic analysis. J Pest Sci 95, 381–395 (2022). https://doi.org/10.1007/s10340-021-01381-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01381-4