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The insecticidal potential of Piper ribesioides (Piperales: Piperaceae) extracts and isolated allelochemicals and their impact on the detoxification enzymes of Spodoptera exigua (Lepidoptera: Noctuidae)

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Abstract

The dried twigs of Piper ribesioides were used to prepare various extracts in different solvents. Each extract was evaluated for their toxicity against 2nd instar larvae of Spodoptera exigua. The highest acute toxicity was observed for ethyl acetate extract with an LD50 of 3.25 and 2.50 μg/larva and LD90 of 9.19 and 8.15 μg/larva after 24 and 48 h post-treatment after topical application. Piperine, methyl piperate, N-cinnamoyl-(2-phenylethyl) amine, pinostrobin, pinocembrin, cinnamic acid, lemairamin, N,N-Diphenylcinnamide, and methyl cinnamate were isolated from this extract that was toxic to S. exigua larvae. Cinnamic acid was the most active compound with a LD50 of 0.17 μg/larva after 48 h of topical treatment. Piperine was significantly similar in activity (LD50 = 0.19 μg/larva), but toxicity decreased with the change in structural configuration as observed with methyl piperate (LD50 = 0.73 μg/larva). Other compounds were 3 to 11-fold less toxic than cinnamic acid and piperine. Growth of survived S. exigua larvae until adult emergence after topical application was recorded and maximum inhibition of about 70% was observed after the application of cinnamic acid. Egg hatch was only 29.11% after cinnamic acid treatment, compared to 97.38% in controls. Neither induction nor inhibition of detoxification enzymes due to treatment of extracts were statistically significant, however, individual compounds like cinnamic acid, methyl cinnamate, piperine, pinostrobin, pinocembrin, and lemairamin did show a moderate impact on these enzymes.

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References

  • Ahmad, N., Fazal, H., Abbasi, B. H., Farooq, S., Ali, M., & Khan, M. A. (2012). Biological role of Piper nigrum L. (black pepper): A review. Asian Pacific Journal of Tropical Biomedicine, 2(3), S1945–S1953.

    Article  Google Scholar 

  • Amad, S., Yuenyongsawad, S., & Wattanapiromsakul, C. (2017). Investigation of Antitubercular and cytotoxic activities of fruit extract and isolated compounds from Piper retrofractum Vahl. Investigation of Antitubercular and Cytotoxic Activities of Fruit Extract and Isolated Compounds from Piper retrofractum, 14(9), 731–739.

    Google Scholar 

  • Amy, Y. L. C., Tang, S. W., Mohd, A. S., Gwendoline, E. C. L., Mawardi, R., & Kaida, K. (2007). Characterization of flavonoid derivatives from Boesenbergia rotunda (L.). The Malaysian Journal of Analytical Sciences, 11(1), 154–159.

    Google Scholar 

  • Andrés, M. F., Rossa, G. E., Cassel, E., Vargas, R. M. F., Santana, O., Díazd, C. E., & Coloma, A. G. (2017). Biocidal effects of Piper hispidinervum (Piperaceae) essential oil and synergism among its main components. Food and Chemical Toxicology, 9, 1086–1092.

    Article  CAS  Google Scholar 

  • Arufe, M. I., Arellano, J. M., Albendín, G., & Sarasquete, C. (2010). Toxicity of parathion on embryo and yolk-sac larvae of gilthead seabream (Sparus aurata I): Effects on survival, cholinesterase, and carboxylesterase activity. Environmental Toxicology, 25(6), 601–607.

    Article  CAS  PubMed  Google Scholar 

  • Ayil-Gutiérrez, B. A., Sanchez-Teyer, L. F., Vazquez-Flota, F., Monforte-González, M., Tamayo-Ordóñez, Y., Tamayo-Ordóñez, M. C., & River, G. (2018). Biological effects of natural products against Spodoptera spp. Crop Protection, 114, 195–207.

    Article  CAS  Google Scholar 

  • Borges-del-castillo, J., Vazquez-bueno, P., Secundino-lucas, M., Martinez-martir, A. I., & Josephnathan, P. (1984). The N-2-phenylethylcinnamamide from Spilanthes ocymifolia. Phytochemistry, 23(11), 2671–2672.

    Article  CAS  Google Scholar 

  • Bullangpoti, V., Kumrungsee, N., Pluempanupat, W., Kainoh, Y., & Saguanpong, U. (2011). Toxicity of ethyl acetate extract and ricinine from Jatropha gossypifolia senescent leaves against Spodoptera exigua Hubner (Lepidoptera: Noctuidae). Journal of Pesticide Science, 36(2), 260–263.

    Article  CAS  Google Scholar 

  • Campos, E. V. R., Proençaa, P. L. F., Oliveira, L. J., Bakshi, M., Abhilash, P. C., & Fraceto, L. F. (2019). Use of botanical insecticides for sustainable agriculture: Future perspectives. Ecological Indicators, 105, 483–495.

    Article  CAS  Google Scholar 

  • Carvalho, F. P. (2017). Pesticides, environment, and food safety. Food and Energy Security, 6(2), 48–60.

    Article  Google Scholar 

  • Che, W., Shi, T., Akram, W., Choi, J. K., & Lee, J. J. (2013). Insecticide resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) from China. Journal of Economic Entomology., 106(4), 1855–1862.

    Article  CAS  PubMed  Google Scholar 

  • Croteau, R., Kutchan, T. M., & Lewis, N. G. (2000). Biochemistry & Molecular Biology of plants in B. Buchanan, W., Gruissem, & R. Jones (Ed), Natural Products (Secondary Metabolites) (pp.1250-1318). American Society of Plant Physiologists.

  • Ellman, G. L., Courtney, K. D., Andres, V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Phramacology., 7(2), 88–90.

    Article  CAS  Google Scholar 

  • Ferraz, A. B. F., Balbino, J. M., Zini, C. A., Ribeiro, V. L. S., Bordignon, S. A. L., & Poser, G. V. (2010). Acaricidal activity and chemical composition of the essential oil from three Piper species. Parasitology Research., 107, 243–248.

    Article  Google Scholar 

  • Guedes, C. A., Teixeira, V. W., Dutra, K. A., & Navarro, Daniela. M.A.F., Cruz, G.S., Lapa Neto, C.J.C., Correia, A.A., Sandes, J.M., Brayner, F.A., Alves, L.C., Teixeira, A.A.C. (2020). Evaluation of Piper marginatum (Piperales: Piperaceae) oil and Geraniol on the embryonic development of Spodoptera frugiperda (Lepidoptera: Noctuidae) in comparison to formulated products. Journal of Economic Entomology., 113(1), 239–248.

    Article  CAS  PubMed  Google Scholar 

  • Hafeez, M., Liu, S., Jan, S., Ali, B., Shahid, M., Ferrnandez-Grandon, G. M., Nawaz, M., Ahmad, A., & Wang, M. (2018). Gossypol-induced fitness gain and increased resistance to deltamethrin in beet armyworm, Spodoptera exigua (Hübner). Pest Management Science, 75(3), 683–693.

    Article  PubMed  CAS  Google Scholar 

  • Hu, B., Songzhu, H., Huang, H., Wei, Q., Ren, M., Huang, S., Tian, X., & Su, J. (2019). Insecticides induce the co-expression of glutathione S-transferases through T ROS/CncC pathway in Spodoptera exigua. Pesticide Biochemistry Physiology., 155, 58–71.

    Article  CAS  PubMed  Google Scholar 

  • Isman, M. B., Miresmailli, S., & Machial, C. (2011). Commercial opportunities for pesticides based on plant EOs in agriculture, industry and consumer products. Phytochemistry Reviews, 10, 197–204.

    Article  CAS  Google Scholar 

  • Koul, O. (2005). Insect antifeedants. CRC Press: American Chemical Society.

  • Koul, O. (2012). Biodiversity and insect pests: Key issues for sustainable management. In G. M. Gurr, S. D. Wratten, & W. E. Snyder (Eds.), Plant biodiversity as a source for natural products for insect pest management (pp. 85–105). UK: John Wiley & Sons.

    Google Scholar 

  • Koul, O. (2016). Naturally occurring insecticidal toxins. Wallingford: CAB International.

    Book  Google Scholar 

  • Koul, O., Singh, G., Singh, R., Singh, J., Daniewski, W. M., & Berlozecki, S. (2004). Bioefficacy and mode-of-action of some limonoids of salannin group from Azadirachta indica A. Juss and their role in a multicomponent system against lepidopteran larvae. Jornal of Biosciences, 29, 409–416.

    Article  CAS  Google Scholar 

  • Koul, O., Walia, S., & Dhaliwal, G. S. (2008). Essential oils as green pesticides: Potential and constraints. Biopesticide International, 4(1), 63–84.

    Google Scholar 

  • Koul, O., Singh, R., Kaur, B., & Kanda, D. (2013). Comparative study on the behavioral response and acute toxicity of some essential oil compounds and their binary mixtures to larvae of Helicoverpa armigera. Spodoptera litura and Chilo partellus. Industrial Crops and Products., 49, 428–436.

    Article  CAS  Google Scholar 

  • Kraikrathok, C., Ngamsaeng, A., Bullangpoti, V., Pluempanupat, W., & Koul, O. (2013). Bioefficacy of some piperaceae plant extracts against Plutella xylostella L. (Lepidoptera: Plutellidae). Communications in Agricultural and Applied Biological Sciences, 78(2), 305–309.

    CAS  PubMed  Google Scholar 

  • Kumrungsee, N., Pluempanupat, W., Koul, O., & Bullangpoti, V. (2014). Toxicity of essential oil compounds against diamondback moth, Plutella xylostella, and their impact on detoxification enzyme activities. Journal of Pest Science., 87, 721–729.

    Article  Google Scholar 

  • Kumrungsee, N., Wongsa, N., Ruttanakham, D., Ratwattananol, A., Pengsook, A., Manaprasertsak, A., Pluempanuphat, W., Bullangpoti, V., & Koul, O. (2018). Bioefficacy of Piper ribesioides (Piperaceae: Piperales) extracts and isolated Piperine against Aedes aegypti (Diptera:Culicidae) larvae and their impact on detoxification enzymes. Biopesticide International, 14(1), 23–30.

    Google Scholar 

  • Lengai, G. M. W., Muthomi, J. W., & Mbega, E. R. (2020). Phytochemical activity and role of botanical pesticides in pest management for sustainable agricultural crop production. Scientific African, 7, e00239.

    Article  Google Scholar 

  • Li, X., Schuler, M. A., & Berenbaum, M. R. (2007). Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52, 231–253.

    Article  PubMed  CAS  Google Scholar 

  • Liangliang, G., Xudong, X., Haijiang, N., Junshan, Y., Guangli, S., Haifeng, W., & Mingliang, Z. (2012). Isolation of cinnamic acid derivatives from the root of Rheum tanguticum Maxim.Ex Balf. And its significance. Journal of Medicinal Plants Research, 6(5), 929–931.

    Google Scholar 

  • LohSiew, F., Muhamad, R., Omar, D., & Rahmani, M. (2011). Insecticidal properties of Piper nigrum fruit extracts and essential oils against Spodoptera litura. International Journal of Agriculture and Biology, 13, 517–522.

    Google Scholar 

  • Manco, G., Porzio, E., & Suzumoto, Y. (2018). Enzymatic detoxification: A sustainable means of degrading toxic organophosphate pesticides and chemical warfare nerve agents. Journal of Chemical Technology and Biotechnology, 93(8), 2064–2082.

    Article  CAS  Google Scholar 

  • Merey, G., & Ana, O. (2011). Copper-catalyzed Bis (methoxycarbonyl) carbene reactions of unsaturated Carboxamides. Helvetica Chimica Acta, 94, 1053–1064.

    Article  CAS  Google Scholar 

  • Moulton, K. J., Pepper, D. A., & Dennehy, T. J. (2000). Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Management Science., 56, 842–848.

    Article  CAS  Google Scholar 

  • Murcia-Meseguer, A., Alves, T. J. S., Budia, F., Ortiz, A., & Medina, P. (2018). Insecticidal toxicity of thirteen commercial plant essential oils against Spodoptera exigua (Lepidoptera: Noctuidae). Phytoparasitica., 46, 233–245.

    Article  CAS  Google Scholar 

  • Nobsathian, S., Bullangpoti, V., Kumrungsee, N., Wongsa, N., & Ruttanakum, D. (2018). Larvicidal effect of compounds isolated from Maerua siamensis (Capparidaceae) against Aedes aegypti (Diptera:Culicidae) larvae. Chemical and Biological Technologies in Agriculture, 5:8, 7. https://doi.org/10.1186/s40538-018-0120-5.

    Article  CAS  Google Scholar 

  • Ntalli, N., Kopiczko, A., Radtke, K., Marciniak, P., Rosinski, G., & Adamski, Z. (2014). Biological activity of Melia azedarach extracts against Spodoptera exigua. Biologia, 69, 1606–1614.

    Article  Google Scholar 

  • Packiam, S. M., Baskar, K., & lgnacimuthu, S. (2014). Feeding deterrent and growth inhibitory activities of PONNEEM, a newly developed phytopesticidal formulation against Helicoverpa armigera (Hubner). Asian Pacific Journal of Tropical Biomedicine, 1(4), S323–S328.

    Article  Google Scholar 

  • Parmar, V. S., Jain, S. C., Bisht, K. S., Taneja, P., Jha, A., Tyaki, O. D., Prasad, A. K., Wengel, J., Olsen, C. E., & Boll, P. M. (1997). Phytochemistry of the genus Piper. Phytochemistry, 46(4), 597–673.

  • Pavela, R. (2012). Sublethal effects of some essential oils on the cotton leaf worm Spodoptera littoralis (Boisduval). Journal of Essential Oil Bearing Plants, 15(1), 144–156.

    Article  CAS  Google Scholar 

  • Pavela, R. (2016). History, Presence and Perspective of Using Plant Extracts as Commercial Botanical Insecticides and Farm Products for Protection against Insects – a Review. Plant Protect. Science, 52(4), 229–241.

    Article  CAS  Google Scholar 

  • Ramsey, J. S., Rider, D. S., Walsh, T. K., De Vos, M., Gordon, K. H. J., Ponnala, L., Macmil, S. L., Roe, B. A., & Jander, G. (2010). Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Molecular Biology, 19(S2), 155–164.

    Article  CAS  PubMed  Google Scholar 

  • Ruangrungsi, N., Prathanturarug, S., Lange, G. L., & Organ, M. G. (1992). An N-Methyl aristolactum and an oxygenated cyclohexane derivatived from Piper ribesioides. Phytochemistry, 31(7), 2397–2400.

    Article  CAS  Google Scholar 

  • Salim, A. M. A., Shakeel, M., Ji, J., Kang, T., Zhang, Y., Ali, E., Xiao, Z., Lu, Y., Wan, H., & Li, J. (2017). Cloning, expression, and functional analysis of two acetylcholinesterase genes in Spodoptera litura (Lepidoptera: Noctuidae). Comparative Biochemistry and Physiology, 206, 16–25.

    Article  CAS  PubMed  Google Scholar 

  • Salleh., W. M. N. H. W., Ahmad, F., & Khong, H. Y. (2014). Chemical composition of Piper stylosum Miq. and Piper ribesioides Wall.essential oils, and their antioxidant, antimicrobial and tyrosinase inhibition activities. Boletín Latinoamericano y del Caribe de Plantas Medicinalesy Aromáticas, 13(5), 488–497.

    Google Scholar 

  • Scott, I. M., Jensen, H. R., Philogene, B. J. R., & Arnason, J. T. (2008). A review of Piper spp. (Piperaceae) phytochemistry, insecticidal activity and mode of action. Phytochem Reviews, 7, 65–75.

  • Shaza, S., & Joumaa, M. (2016). Isolation and Identification of Methyl cinnamate from Syrian Ocimum basilicum. Chemistry and Materials Research, 8(6), 13–19.

    Google Scholar 

  • Simeon, K. A., Tiwalade, A. O., Doye, D. A., & Dieter, J. V. W. (1997). New Amides from Zanthoxylum lemairie Pericarps. Planta Medica, 63, 286–287.

    Article  Google Scholar 

  • Singh, R., Koul, O., Pushpinder, J., Jawala, R., & Jindal, J. (2009). Toxicity of some essential oil constituents and their binary mixtures against Chilopartellus Swinhoe (Lepidoptera: Pyralidae). International Journal of Tropical Insect Science, 29, 93–101.

    Article  CAS  Google Scholar 

  • Smagghe, G., Pineda, S., Carton, B., Estal, P. D., Budia, F., & Vinuela, E. (2003). Toxicity and kinetics of methoxyfenozide ingreenhouse-selected Spodoptera exigua (Lepidoptera: Noctuidae). Pest Management Science., 59, 1203–1209.

    Article  CAS  PubMed  Google Scholar 

  • Sudmoon, R., Tanee, T., Wongpanich, V., Bletter, N., & Chaveerach, A. (2012). Ethnobotany and species specific molecular markers of some medicinal sakhan (Piper, Piperaceae). Journal of Medicinal Plants Research, 6(7), 1168–1175.

  • Tetsuo, N., Jun, W., Jun, K., & Ryoya, N. (1997). Isolation and Activity of N-p-Coumaroyltyramine,an α-Glucosidase Inhibitor in Welsh Onion (Allium fistulosum). Bioscience, Biotechnology, and Biochemistry, 61(7), 1138–1141.

    Article  Google Scholar 

  • Tharamak, Pengsook, A., Ratwatthananon, A., Kumrungsee, N., Bullangpoti, V., & Pluempanupat, W. (2019). Synthesis of thymyl esters and their insecticidal activity against Spodoptera litura (Lepidoptera: Noctuidae). Pest Management Science, 76, 928–935.

    Article  PubMed  CAS  Google Scholar 

  • Torres-Pelayo, V. R., Fernandez, M. S., Carmona-Hernandez, O., Molina-Torres, J., & Lozada-Garcia, J. A. (2016). A phytochemical and ethnopharmacological review of the genus piper: as a potent bio-insecticide. Research & Reviews: Research Journal of Biology, 4, 45–51.

  • Ware, G. W., & Whitacre, D. M. (2004). History of Pesticides. The Pesticide Book (6th ed.). Willoughby: MeisterPro In- formation Resources.

    Google Scholar 

  • Xiang, C.-P., Shi, Y.-N., Liu, F.-F., Lia, H.-Z., Zhang, Y.-J., Yang, C.-R., & Xu, M. (2016). Survey of the chemical compounds of Piper spp. (Piperaceae) and their biological activities. Natural Product Communications, 11, 1403–1408.

    PubMed  Google Scholar 

  • Zhang, Y. N., He, P., Xue, J. P., Guo, Q., Zhu, X. Y., Fang, L. P., & Li, J. B. (2017). Insecticidal activities and biochemical properties of Pinellia ternata extracts against the beet armyworm Spodoptera exigua. Journal of Asia-Pacific Entomology, 20, 469–476.

    Article  Google Scholar 

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Acknowledgements

This research was supported by Agricultural Research Development Agency (Public Organization) (Contract No.CPR6005020310). N.K.thanks Zoology Department and Chemistry Department, Faculty of Science, Kasetsart University for support and use of analytical equipment for this research. Thanks are also due to Rajamangala University of Technology Thanyaburi for help during this investigation. Authors also thank Miss Benjawan Dunkhunthod, School of Preclinic, Institute of Science, Suranaree University of Technology, Nokhon Ratchasima for specific advice in statistical analysis. S.K. and Nakhonsawan Campus Mahidol University thank Professor Patoomratana Tuchinda and Mr.Wisuwat Thongpichai for their advice and valuable discussion during this research. V.B. is grateful to Franco for financial support.

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Authors and Affiliations

  1. Mahidol University Nakhonsawan Campus, Nakhonsawan, 60130, Thailand

    Saksit Nobsathian

  2. Institute of Research and Development, Rajamangala University of Technology, Thanyaburi, Pathumthani, 12110, Thailand

    Chatwadee Saiyaitong

  3. Insect Biopesticide Research Centre, 30 Parkash Nagar, Jalandhar, 144003, India

    Opender Koul

  4. Animal Toxicology and Physiology Speciality Research Unit, Zoology Department, Faculty of Science, Kasetsart University, Bangkok, 10900, Thailand

    Opender Koul & Vasakorn Bullangpoti

  5. Special Research Unit for Advanced Magnetic Resonance, Department of Chemistry and Center of Excellence for Innovation in Chemistry, Faculty of Science, Kasetsart University, Bangkok, 10900, Thailand

    Wanchai Pluempanupat

  6. Biology Department, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Khlong Hok, Pathumthani, 12110, Thailand

    Nutchaya Kumrungsee

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  1. Saksit Nobsathian
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Nutchaya Kumrungsee: Conceptualization, Methodology, Investigation, Writing -original draft, Project administration.Chatwadee Saiyaithong: Visualization. Opender Koul: Experimental advice, Writing-review& Editing. Wanchai Pluempanupat: Resources. Vasakorn Bullangpoti:Resources. Saksit Nobsathian: Writing - Original Draft, Resources.

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Nobsathian, S., Saiyaitong, C., Koul, O. et al. The insecticidal potential of Piper ribesioides (Piperales: Piperaceae) extracts and isolated allelochemicals and their impact on the detoxification enzymes of Spodoptera exigua (Lepidoptera: Noctuidae). Phytoparasitica 49, 659–673 (2021). https://doi.org/10.1007/s12600-021-00891-2

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