Skip to main content
Log in

Synergistic interactions among the major constituents of lemongrass essential oil against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni

  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Since plant essential oils are composed with vast numbers of constituents, they often show complex interactions among the components. Although the research interest on the insecticidal activity of plant essential oils has been gaining more attention recently, most of the studies still focus on simple screening of active plant source or identification of active compounds. In the present study, insecticidal activity and synergistic interactions among the four major constituents of lemongrass (Cymbopogon citratus) essential oil were examined via topical application against the third instar larvae of the cabbage looper, Trichoplusia ni. Two synergistic binary combinations—citral + limonene and citral + geranyl acetate—were identified at the equivalent mixing ratios. The former was especially synergistic in larvae and additionally with respect to cytotoxicity in the ovarian cell line of the cabbage looper. Morphological observations indicated different cytotoxic modes of action of citral and limonene. GC–MS analysis of larval extracts in vivo revealed several metabolites of citral and limonene, with geranic acid and neric acid (from citral), and limonene-1,2-diol (from limonene) as the major ones. The insecticidal activity of geranic acid was very similar to that of the parent compound, citral, but limonene-1,2-diol failed to show any toxicity, indicating that inhibition of the metabolism could be a good strategy to enhance toxicity. Further, larval extracts following topical administration of a binary mixture of the two compounds revealed higher internal concentrations of both compared to their individual application, suggesting the possibility of enhanced cuticular penetration as the mechanism of synergy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahluwalia V, Sisodia R, Walia S, Sati OP, Kumar J, Kundu A (2014) Chemical analysis of essential oils of Eupatorium adenophorum and their antimicrobial, antioxidant and phytotoxic properties. J Pest Sci 87:341–349. doi:10.1007/s10340-013-0542-6

    Article  Google Scholar 

  • Akhtar Y, Pages E, Stevens A, Bradbury R, da Camara CAG, Isman MB (2012) Effect of chemical complexity of essential oils on feeding deterrence in larvae of the cabbage looper. Physiol Entomol 37:81–91. doi:10.1111/j.1365-3032.2011.00824.x

    Article  CAS  Google Scholar 

  • Aqil M, Ahad A, Sultana Y, Ali A (2007) Status of terpenes as skin penetration enhancers. Drug Discov Today 12:1061–1067. doi:10.1016/j.drudis.2007.09.001

    Article  CAS  PubMed  Google Scholar 

  • Arellano A, Santoyo S, Martin C, Ygartua P (1996) Enhancing effect of terpenes on the in vitro percutaneous absorption of diclofenac sodium. Int J Pharm 130:141–145. doi:10.1016/0378-5173(95)04364-0

    Article  CAS  Google Scholar 

  • Baldin ELL, Crotti AEM, Wakabayashi KAL, Silva JPGF, Aguiar GP, Souza ES, Veneziani RCS, Groppo M (2013) Plant-derived essential oils affecting settlement and oviposition of Bemisia tabaci (Genn.) biotype B on tomato. J Pest Sci 86:301–308. doi:10.1007/s10340-012-0462-x

    Article  Google Scholar 

  • Bekele J, Hassanali A (2001) Blend effects in the toxicity of the essential oil constituents of Ocimum kilimandscharicum and Ocimum kenyense (Labiateae) on two post-harvest insect pests. Phytochemistry 57:385–391. doi:10.1016/S0031-9422(01)00067-X

    Article  CAS  PubMed  Google Scholar 

  • Belletti N, Kamdem SS, Tabanelli G, Lanciotti R, Gardini F (2010) Modeling of combined effects of citral, linalool and β-pinene used against Saccharomyces cerevisiae in citrus-based beverages subjected to a mild heat treatment. Int J Food Microbiol 136:283–289. doi:10.1016/j.ijfoodmicro.2009.10.030

    Article  CAS  PubMed  Google Scholar 

  • Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94:223–253. doi:10.1016/j.ijfoodmicro.2004.03.022

    Article  CAS  PubMed  Google Scholar 

  • Carlson LHC, Machado RAF, Spricigo CB, Pereira LK, Bolzan A (2001) Extraction of lemongrass essential oil with dense carbon dioxide. J Supercrit Fluids 21:33–39. doi:10.1016/S0896-8446(01)00085-7

    Article  CAS  Google Scholar 

  • Chami F, Chami N, Bennis S, Bouchikhi T, Remmal A (2005) Oregano and clove essential oils induce surface alteration of Saccharomyces cerevisiae. Phytother Res 19:405–408. doi:10.1002/ptr.1528

    Article  CAS  PubMed  Google Scholar 

  • Chang KS, Shin EH, Park C, Ahn YJ (2012) Contact and fumigant toxicity of Cyperus rotundus steam distillate constituents and related compounds to insecticide-susceptible and -resistant Blattella germanica. J Med Entomol 49:631–639. doi:10.1603/ME11060

    Article  CAS  PubMed  Google Scholar 

  • Costa CA, Kohn DO, de Lima VM, Gargano AC, Flório JC, Costa M (2011) The GABAergic system contributes to the anxiolytic-like effect of essential oil from Cymbopogon citratus (lemongrass). J Ethnopharmacol 137:828–836. doi:10.1016/j.jep.2011.07.003

    Article  CAS  PubMed  Google Scholar 

  • Cox SD, Mann CM, Markham JL, Bell HC, Gustafson JE, Warmington JR, Wyllie SG (2001) The mode of antimicrobial action of the essential oil of Melaleuca alternifolia (tea tree oil). J Appl Microbiol 88:170–175. doi:10.1046/j.1365-2672.2000.00943.x

    Article  Google Scholar 

  • Devi KP, Nisha SA, Sakthivel R, Pandian SK (2010) Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 130:107–115. doi:10.1016/j.jep.2010.04.025

    Article  CAS  PubMed  Google Scholar 

  • Di Pasqua R, Betts G, Hoskins N, Edwards M, Ercolini D, Mauriello G (2007) Membrane toxicity of antimicrobial compounds from essential oils. J Agric Food Chem 55:4863–4870. doi:10.1021/jf0636465

    Article  PubMed  Google Scholar 

  • Diliberto JJ, Srinivas P, Overstreet D, Usha G, Burka LT, Birnbaum S (1990) Metabolism of citral, an alpha, beta-unsaturated aldehyde, in male F344 rats. Drug Metab Dispos 18:866–875

    CAS  PubMed  Google Scholar 

  • Dragicevic-Curic N, Scheglmann D, Albrecht V, Fahr A (2008) Temoporfin-loaded invasomes: development, characterization and in vitro skin penetration studies. J Control Release 127:59–69. doi:10.1016/j.jconrel.2007.12.013

    Article  CAS  PubMed  Google Scholar 

  • Dudai N, Larkov O, Putievsky E, Lerner HR, Ravid U, Lewinsohn E, Mayer AM (2000) Biotransformation of constituents of essential oils by germinating wheat seed. Phytochemistry 55:375–382. doi:10.1016/S0031-9422(00)00333-2

    Article  CAS  PubMed  Google Scholar 

  • Fields PG, Woods S, Taylor WG (2010) Triterpenoid saponins synergize insecticidal pea peptides: effect on feeding and survival of Sitophilus oryzae (Coleoptera: Curculionidae). Can Entomol 142:501–512. doi:10.4039/n10-024

    Article  Google Scholar 

  • Gisi U, Binder H, Rimbach E (1985) Synergistic interactions of fungicides with different modes of action. Trans Br Mycol Soc 85:299–306. doi:10.1016/S0007-1536(85)80192-3

    Article  CAS  Google Scholar 

  • Hsu WS, Yen JH, Wang YS (2013) Formulas of components of citronella oil against mosquitoes (Aedes aegypti). J Environ Sci Heal B 48:1014–1019. doi:10.1080/03601234.2013.816613

    Article  CAS  Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66. doi:10.1146/annurev.ento.51.110104.151146

    Article  CAS  PubMed  Google Scholar 

  • Isman MB, Wilson JA, Bradbury R (2008) Insecticidal activities of commercial rosemary oils (Rosmarinus officinalis) against larvae of Pseudaletia unipuncta and Trichoplusia ni in relation to their chemical compositions. Pharm Biol 46:82–87. doi:10.1080/13880200701734661

    Article  CAS  Google Scholar 

  • Jiang Z, Akhtar Y, Bradbury R, Zhang X, Isman MB (2009) Comparative toxicity of essential oils of Litsea pungens and Litsea cubeba and blends of their major constituents against the cabbage looper, Trichoplusia ni. J Agric Food Chem 57:4833–4837. doi:10.1021/jf900274r

    Article  CAS  PubMed  Google Scholar 

  • Kanikkannan N, Andega S, Burton S, Babu RJ, Singh M (2004) Formulation and in vitro evaluation of transdermal patches of melatonin. Drug Dev Ind Pharm 30:205–212. doi:10.1081/DDC-120028716

    Article  CAS  PubMed  Google Scholar 

  • Kendra PE, Montgomery WS, Niogret J, Schnell EQ, Deyrup MA, Epsky ND (2014) Evaluation of seven essential oils identifies cubeb oil as most effective attractant for detection of Xyle6borus glabratus. J Pest Sci 87:681–689. doi:10.1007/s10340-014-0561-y

    Article  Google Scholar 

  • Kim SW, Kang J, Park IK (2013) Fumigant toxicity of Apiaceae essential oils and their constituents against Sitophilus oryzae and their acetylcholinesterase inhibitory activity. J Asia Pac Entomol 16:443–448. doi:10.1016/j.aspen.2013.07.002

    Article  CAS  Google Scholar 

  • Korenblum E, de Vasconcelos Goulart FR, de Almeida Rodrigues I, Abreu F, Lins U, Alves PB, Blank AF, Valoni E, Sebastián GV, Alviano DS, Alviano CS, Seldin L (2013) Antimicrobial action and anti-corrosion effect against sulfate reducing bacteria by lemongrass (Cymbopogon citratus) essential oil and its major component, the citral. AMB Express 3:44. doi:10.1186/2191-0855-3-44

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar P, Mishra S, Malik A, Satya S (2013) Housefly (Musca domestica L.) control potential of Cymbopogon citratus Stapf. (Poales: Poaceae) essential oil and monoterpenes (citral and 1,8-cineole). Parasitol Res 112:69–76. doi:10.1007/s00436-012-3105-5

    Article  PubMed  Google Scholar 

  • Miresmailli S, Bradbury R, Isman MB (2006) Comparative toxicity of Rosmarinus officinalis L. essential oil and blends of its major constituents against Tetranychus urticae Koch (Acari: Tetranychidae) on two different host plants. Pest Manag Sci 62:366–371. doi:10.1002/ps.1157

    Article  CAS  PubMed  Google Scholar 

  • Miyazawa M, Wada T, Kameoka H (1998) Biotransformation of (+)- and (−)-limonene by the larvae of common cutworm (Spodoptera litura). J Agric Food Chem 46:300–303. doi:10.1021/jf970142l

    Article  CAS  PubMed  Google Scholar 

  • Miyazawa M, Shindo M, Shimada T (2002) Sex differences in the metabolism of (+)- and (−)-limonene enantiomers to carveol and perillyl alcohol derivatives by cytochrome P450 enzymes in rat liver microsomes. Chem Res Toxicol 15:15–20. doi:10.1021/tx0155350

    Article  CAS  PubMed  Google Scholar 

  • Papachristos DP, Karamanoli KI, Stamopoulos DC, Menkissoglu-Spiroudi U (2004) The relationship between the chemical composition of three essential oils and their insecticidal activity against Acanthoscelides obtectus (Say). Pest Manag Sci 60:514–520. doi:10.1002/ps.798

    Article  CAS  PubMed  Google Scholar 

  • Pavela R (2014) Acute, synergistic and antagonistic effects of some aromatic compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) larvae. Ind Crops Prod 60:247–258. doi:10.1016/j.indcrop.2014.06.030

    Article  CAS  Google Scholar 

  • Pavela R (2015) Acute toxicity and synergistic and antagonistic effects of the aromatic compounds of some essential oils against Culex quinquefasciatus Say larvae. Parasitol Res 114:3835–3853. doi:10.1007/s00436-015-4614-9

    Article  PubMed  Google Scholar 

  • Rivera-Carriles K, Argaiz A, Palou E, LóPez-Malo A (2005) Synergistic inhibitory effect of citral with selected phenolics against Zygosaccharomyces bailii. J Food Prot 68:602–606

    Article  CAS  PubMed  Google Scholar 

  • Ryan MF, Byrne O (1988) Plant-insect coevolution and inhibition of acetylcholinesterase. J Chem Ecol 14:1965–1975. doi:10.1007/BF01013489

    Article  CAS  PubMed  Google Scholar 

  • Shin S (2005) Anti-salmonella activity of lemongrass oil alone and in combination with antibiotics. Nat Prod Sci 11:160–164

    CAS  Google Scholar 

  • Singh N, Luthra R, Sangwan R (1989) Effect of leaf position and age on the essential oil quantity and quality in lemongrass (Cymbopogon flexuosus). Planta Med 55:254–256. doi:10.1055/s-2006-961997

    Article  CAS  PubMed  Google Scholar 

  • Sousa J, Costa A, Leite M, Guerra F, Silva V, Menezes C, Pereira F, Lima E (2016) Antifungal activity of citral by disruption of ergosterol biosynthesis in fluconazole resistant Candida tropicalis. Int J Trop Dis Health 11:1–11. doi:10.9734/IJTDH/2016/21423

    Article  Google Scholar 

  • Subongkot T, Duangjit S, Rojanarata T, Opanasopit P, Ngawhirunpat T (2012) Ultradeformable liposomes with terpenes for delivery of hydrophilic compound. J Liposome Res 22:254–262. doi:10.3109/08982104.2012.690158

    Article  CAS  PubMed  Google Scholar 

  • Tajidin NE, Ahmad SH, Rosenani AB, Azimah H, Munirah M (2012) Chemical composition and citral content in lemongrass (Cymbopogon citratus) essential oil at three maturity stages. Afr J Biotechnol 11:2685–2693. doi:10.5897/AJB11.2939

    Article  CAS  Google Scholar 

  • Tak JH, Isman MB (2015) Enhanced cuticular penetration as the mechanism for synergy of insecticidal constituents of rosemary essential oil in Trichoplusia ni. Sci Rep 5:12690. doi:10.1038/srep12690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tak JH, Isman MB (2016) Metabolism of citral, the major constituent of lemongrass oil, in the cabbage looper, Trichoplusia ni, and effects of enzyme inhibitors on toxicity and metabolism. Pestic Biochem Physiol 133:20–25. doi:10.1016/j.pestbp.2016.03.009

    Article  CAS  PubMed  Google Scholar 

  • Tak JH, Kim HK, Lee SH, Ahn YJ (2006) Acaricidal activities of paeonol and benzoic acid from Paeonia suffruticosa root bark and monoterpenoids against Tyrophagus putrescentiae (Acari: Acaridae). Pest Manag Sci 62:551–557. doi:10.1002/ps.1212

    Article  CAS  PubMed  Google Scholar 

  • Tak JH, Jovel E, Isman MB (2016a) Contact, fumigant, and cytotoxic activities of thyme and lemongrass essential oils against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni. J Pest Sci 89:183–193. doi:10.1007/s10340-015-0655-1

    Article  Google Scholar 

  • Tak JH, Jovel E, Isman MB (2016b) Comparative and synergistic activity of Rosmarinus officinalis L. essential oil constituents against the larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni (Lepidoptera: Noctuidae). Pest Manag Sci 72:474–480. doi:10.1002/ps.4010

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Hu L, Luquette LJ, Gao G, Liu Y, Qu H, Xi R, Lu ZJ, Park PJ, Elledge SJ (2012) Systematic identification of synergistic drug pairs targeting HIV. Nat Biotechnol 30:1125–1130. doi:10.1038/nbt.2391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong F, Coats JR (2012) Quantitative structure-activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag Sci 68:1122–1129. doi:10.1002/ps.3280

    Article  CAS  PubMed  Google Scholar 

  • Wen H, Zhang Q, Cheng D, Zhang Z, Xu H, Song X (2013) Cassia oil as a substitute solvent for xylene for rotenone EC and its synergistic activities. Pestic Biochem Physiol 105:189–196. doi:10.1016/j.pestbp.2013.02.002

    Article  CAS  Google Scholar 

  • Williams AC, Barry BW (2012) Penetration enhancers. Adv Drug Deliv Rev 64:128–137. doi:10.1016/j.addr.2012.09.032

    Article  Google Scholar 

  • Zheljazkov VD, Cantrell CL, Astatkie T, Cannon JB (2011) Lemongrass productivity, oil content, and composition as a function of nitrogen, sulfur, and harvest time. Agron J 103:805–812. doi:10.2134/agronj2010.0446

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Nancy Brad, Zyta Abramowski, and Lina Madilao for technical support.

Funding

The present study was funded by a University of British Columbia graduate fellowship (to JHT), a Discovery grant from the Natural Sciences and Engineering Research Council of Canada (NSERC; 2729-11)(to MBI), a Canada International Food Security Research Fund grant from the International Development Research Fund (IDRC; 106526)(to EJ), and a collaborative grant from Kittrich Corporation (to MBI).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Murray B. Isman.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human rights statement

This article does not contain any studies with human participants performed by any of the authors.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tak, JH., Jovel, E. & Isman, M.B. Synergistic interactions among the major constituents of lemongrass essential oil against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni . J Pest Sci 90, 735–744 (2017). https://doi.org/10.1007/s10340-016-0827-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0827-7

Keywords

Navigation