Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-17T04:02:08.411Z Has data issue: false hasContentIssue false
  • English
  • Français

Triterpenoid saponins synergize insecticidal pea peptides: effect on feeding and survival of Sitophilus oryzae (Coleoptera: Curculionidae)

Published online by Cambridge University Press:  02 April 2012

Paul G. Fields ,
Sheila Woods  and
Wesley G. Taylor
Paul G. Fields*
Affiliation:
Cereal Research Centre, Agriculture and Agri-Food Canada, 195 Dafoe Road, Winnipeg, Manitoba, Canada R3T 2M9
Sheila Woods
Affiliation:
Cereal Research Centre, Agriculture and Agri-Food Canada, 195 Dafoe Road, Winnipeg, Manitoba, Canada R3T 2M9
Wesley G. Taylor
Affiliation:
Saskatoon Research Centre, Agriculture and Agri-Food Canada, 107 Science Place, Saskatoon, Saskatchewan, Canada S7N 0X2
*
1 Corresponding author (e-mail: paul.fields@agr.gc.ca).
Get access Rights & Permissions [Opens in a new window]

Abstract

The triterpenoid saponins soyasaponin I, dehydrosoyasaponin I, echinocystic acid 3-glucoside, β-escin, glycyrrhizic acid, hederacoside C, and α-hederin were tested alone and in combination with insecticidal PA1b peptide mixtures isolated from peas for their effects on the feeding and survival of a stored-product insect, the rice weevil, Sitophilus oryzae (L.). There were two sources of peptides: a purified extract composed primarily of PA1b peptides and a partially purified extract (C8 extract) that contained mainly peptides and lesser amounts of soyasaponin I, dehydrosoyasaponin I, and other compounds. Dehydrosoyasaponin I, echinocystic acid 3-glucoside, α-hederin, and β-escin were active (causing reduced feeding and increased mortality) when used alone. Soyasaponin I, hederacoside C, and glycyrrhizic acid were inactive when used alone. Purified peptides and C8 extract were active when used alone. The mixtures of the inactive soyasaponin I and the active peptides were as active as peptides alone, even when peptides composed only 10% of the mixture. Similar trends were seen with the mixtures of β-escin and PA1b. In general, the mixtures of saponins and peptides were synergistic. Possible modes of synergistic action are discussed.

Résumé

Nous avons testé les effets sur l'alimentation et la survie d'un insecte des produits entreposés, le charançon du riz, Sitophilus oryzae (L.), de saponines triterpénoïdes, soit la sojasaponine I, la déshydrosaponine I, le glucoside-3 de l'acide échinocystique, la β-escine, l'acide glycyrrhizique, l'hédéracoside C et l'α-hédérine, seules ou en combinaison avec des mélanges de peptides PA1b insecticides extraits de pois. Il y avait deux sources de peptides, un extrait purifié composé principalement de peptides PA1b et un extrait partiellement purifié (extrait C8) qui contenait surtout des peptides et des quantités moindres de sojasaponine I, de déshydrosaponine I et d'autres composés. Utilisés seuls, la déydrosaponine I, le glucoside-3 de l'acide éinocystique, l'α-hédérine et la β-escine sont des produits actifs (ils réduisent l'alimentation et augmentent la mortalité). La sojasaponine I, l'hédéracoside C et l'acide glycyrrhizique seuls restent inactifs. Les peptides purifiés et l'extrait C8 sont actifs seuls. Le mélange de sojasaponine I inactive et de peptides actifs a une action égale à celle des peptides seuls, même lorsque les peptides ne représentent que 10% du mélange. Des tendances semblables s'observent avec les mélanges de β-escine et de PA1b. En général, les mélanges de saponines et de peptides produisent une synergie. Nous discutons des modes possibles de cette action synergique.

[Traduit par la Rédaction]

Type
Articles
Information
The Canadian Entomologist , Volume 142 , Issue 5 , October 2010 , pp. 501 - 512
Copyright
Copyright © Entomological Society of Canada 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Applebaum, S.L., and Birk, Y. 1979. Saponins. In Herbivores: their interaction with secondary plant metabolites. Edited by Rosenthal, G.A. and Janzen, D.H.Academic Press Inc., New York. pp. 539–566.Google Scholar
Banks, H.J., and Fields, P.G. 1995. Physical methods for insect control in stored grain. In Stored grain ecosystems. Edited by Jayas, D.S., White, N.D.G., Muir, W.E., and Sinha, R.H.. Marcel Dekker Inc., New York. pp. 353–409.Google Scholar
Bell, E.A. 1978. Toxins in seeds. In Biochemical aspects of plant and animal coevolution. Edited by Harborne, J.B.Academic Press Inc., New York. pp. 143–161.Google Scholar
Bliss, C.I. 1939. The toxicity of poisons applied jointly. Annals of Applied Biology, 26: 585–615. doi:10.1111/j.1744-7348.1939.tb06990.x.CrossRefGoogle Scholar
Bodnaryk, R., Fields, P.G., Xie, Y., and Fulcher, K. 1999. Insecticidal factor from field peas. United States Patent No. 5,955,082.Google Scholar
Brindley, W.A., and Selim, A.A. 1984. Synergism and antagonism in the analysis of insecticide resistance. Environmental Entomology, 13: 348–354.CrossRefGoogle Scholar
Coombs, C.W., Billings, C.J., and Porter, J.E. 1977. The effect of yellow split-peas (Pisum sativum L.) and other pulses on the productivity of certain strains of Sitophilus oryzae (L.) (Col. Curculionidae) and the ability of other strains to breed thereon. Journal of Stored Products Research, 13: 53–58. doi:10.1016/0022-474X(77)90058-3.CrossRefGoogle Scholar
Delobel, B., Grenier, A., Gueguen, J., Ferrasson, E., and Mbailao, M. 1999. Utilisation d'un polypeptide dérivé d'une albumine PA1b de légumineuse comme insecticide. French Patent No. 98 05877.Google Scholar
Fields, P.G. 2006. Effect of Pisum sativum fractions on the mortality and progeny production of nine stored grain insects. Journal of Stored Products Research, 42: 86–96. doi:10.1016/j.jspr.2004.11.005.CrossRefGoogle Scholar
Fields, P.G., and White, N.D.G. 2002. Alternatives to methyl bromide treatments for stored product and quarantine insects. Annual Review of Entomology, 47: 331–359. PMID:11729078 doi:10.1146/annurev.ento.47.091201.145217.CrossRefGoogle ScholarPubMed
Fields, P.G., Xie, Y.S., and Hou, X. 2001. Repellent effect of pea (Pisum sativum) fractions against stored-product insects. Journal of Stored Products Research, 37: 359–370. PMID:11463398 doi:10.1016/S0022-474X(00)00038-2.CrossRefGoogle ScholarPubMed
Fong, W.G., Moye, H.A., Seiber, J.N., and Toth, J.P. 1999. Pesticide residues in food. John Wiley & Sons, Inc., New York.Google Scholar
Francis, G., Kerem, Z., Makkar, H.P.S., and Becker, K. 2002. The biological action of saponins in animal systems: a review. British Journal of Nutrition, 88: 587–605. PMID:12493081 doi:10.1079/BJN2002725.CrossRefGoogle ScholarPubMed
Golob, P., Dales, M., Fidgen, A., Evans, J., and Gudrups, I. 1999. The use of spices and medicinals as bioactive protectants for grains. Food and Agricultural Organisation of the United Nations, Rome, Italy.Google Scholar
Gressent, F., Rahioui, I., and Rahbe, Y. 2003. Characterization of a high-affinity binding site for the pea albumin 1b entomotoxin in the weevil Sitophilus. European Journal of Biochemistry, 270: 2429–2435. PMID:12755698 doi:10.1046/j.1432-1033.2003.03611.x.CrossRefGoogle ScholarPubMed
Gruber, C.W., Cemazar, M., Anderson, M.A., and Craik, D.J. 2007. Insecticidal plant cyclotides and related cystine knot toxins. Toxicon, 49: 561–575. PMID:17224167 doi:10.1016/j.toxicon.2006.11.018.CrossRefGoogle ScholarPubMed
Higgins, T.J.V., Chandler, P.M., Randall, P.J., Spencer, D., Beach, L.R., Blagrove, R.J., Kortt, A.A., and Inglis, A.S. 1986. Gene structure, protein structure, and regulation of the synthesis of a sulfur-rich protein in pea seeds. Journal of Biological Chemistry, 261: 11124–11130. PMID:3755437.CrossRefGoogle ScholarPubMed
Holloway, G.J. 1986. The potency and effect of phytotoxins within yellow split-pea (Pisum sativum) and adzuki bean (Vigna angularis) on survival and reproductive potential of Sitophilu oryzae (L.) (Coleoptera: Curculionidae). Bulletin of Entomological Research, 76: 287–295. doi:10.1017/S0007485300014759.CrossRefGoogle Scholar
Hou, X., and Fields, P.G. 2003 a. Effectiveness of protein-rich pea flour for the control of stored-product beetles. Entomologia Experimentalis et Applicata, 108: 125–131. doi:10.1046/j.1570-7458.2003.00074.x.CrossRefGoogle Scholar
Hou, X., and Fields, P.G. 2003 b. Granary trial of protein-enriched pea flour for the control of three stored-product insects in barley. Journal of Economical Entomology, 96: 1005–1015. PMID: 12852648 doi:10.1603/0022-0493-96.3.1005.CrossRefGoogle ScholarPubMed
Hou, X., Fields, P., and Taylor, W. 2004. Combination of protein-rich pea flour and pea extract with insecticides and enzyme inhibitors for control of stored-product beetles. The Canadian Entomologist, 136: 581–590. doi:10.4039/N03-077.CrossRefGoogle Scholar
Hou, X., Taylor, W.G., and Fields, P.G. 2006. Effect of pea flour and pea flour extracts on Sitophilus oryzae. The Canadian Entomologist, 138: 95–103. doi:10.4039/N05-023.CrossRefGoogle Scholar
Jayasinghe, U.L.B., and Fujimoto, Y. 1999. Insecticidal saponin from Pometia eximia. Fitoterapia, 70: 87–88. doi:10.1016/S0367-326X(98)00008-2.CrossRefGoogle Scholar
Johnson, J.H., Bloomquist, J.R., Krapcho, K.J., Krat, R.M. Jr, Trovato, R., Eppler, K.G., Morgan, T.K., and DelMar, E.G. 1998. Novel insecticidal peptides from Tegenaria agrestis spider venom may have a direct effect on the insect central nervous system. Archives of Insect Biochemistry and Physiology, 38: 19–31. PMID: 9589602 doi:10.1002/(SICI)1520-6327(1998)38:1,19::AID-ARCH3.3.0.CO;2-Q.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Jouvensal, L., Quillien, L., Ferrasson, E., Rahbe, Y., Gueguen, J., and Vovelle, F. 2003. Pa1b, an insecticidal protein extracted from pea seeds (Pisum sativum): H-1-2-D NMR study and molecular modeling. Biochemistry, 42: 11915–11923. PMID:14556622 doi:10.1021/bi034803l.CrossRefGoogle ScholarPubMed
Khalil, A.H., and El-Adawy, T.A. 1994. Isolation, identification and toxicity of saponin from different legumes. Food Chemistry, 50: 197–201. doi:10.1016/0308-8146(94)90120-1.CrossRefGoogle Scholar
Lacaille-Dubois, M.A., and Wagner, H. 1996. A review of the biological and pharmacological activities of saponins. Phytomedicine, 2: 363–386.CrossRefGoogle ScholarPubMed
Marquina, S., Maldonado, N., Garduño-Ramírez, M.L., Aranda, E., Villarreal, M.L., Navarro, V., Bye, R., Delgado, G., and Alvarez, L. 2001. Bioactive oleanolic acid saponins and other constituents from the roots of Viguiera decurrens. Phytochemistry, 56: 93–97. PMID:11198824 doi:10.1016/S0031-9422(00)00283-1.CrossRefGoogle ScholarPubMed
Metcalf, R.L. 1967. Mode of action of insecticide synergists. Annual Review of Entomology, 12: 229–256. PMID:5340719 doi:10.1146/annurev.en.12.010167.001305.CrossRefGoogle ScholarPubMed
Osbourn, A. 1996. Saponins and plant defence—a soap story. Trends in Plant Science, 1: 4–9. doi: 10.1016/S1360-1385(96)80016-1.CrossRefGoogle Scholar
Pelah, D., Abramovich, Z., Markus, A., and Wiesman, Z. 2002. The use of commercial saponin from Quillaja saponaria bark as a natural larvicidal agent against Aedes aegypti and Culex pipiens. Journal of Ethnopharmacology, 81: 407–409. PMID:12127245 doi:10.1016/S0378-8741(02)00138-1.CrossRefGoogle ScholarPubMed
Peyronnet, O., Noulin, J., Laprade, R., and Schwartz, J. 2004. Patch-clamp study of the apical membrane of the midgut of Manduca sexta larvae: direct demonstration of endogenous channels and effect of a Bacillus thuringiensis toxin. Journal of Insect Physiology, 50: 791–803. PMID:15350500 doi:10.1016/j.jinsphys.2004.05.013.CrossRefGoogle ScholarPubMed
Price, K.R., and Fenwick, G.R. 1987. The chemistry and biological significance of saponins in foods and feedingstuffs. Critical Reviews in Food Science and Nutrition, 26: 27–125. PMID: 3308321 doi:10.1080/10408398709527461.CrossRefGoogle ScholarPubMed
Rahman, A., Ahamed, A., Amakawa, T., Goto, N., and Tsurumi, S. 2001. Chromosaponin I specifically interacts with AUX1 protein in regulating the gravitropic response of Arabidopsis roots. Plant Physiology, 125: 990–1000. PMID:11161055 doi:10.1104/pp.125.2.990.CrossRefGoogle ScholarPubMed
Renault, S., De Lucca, A.J., Boue, S., Bland, J.M., Vigo, C.B., and Selitrennikoff, C.P. 2003. CAY-1, a novel antifungal compound from cayenne pepper. Medical Mycology, 41: 75–82. PMID:12627807.CrossRefGoogle ScholarPubMed
Robertson, J.L., and Smith, K.C. 1984. Joint action of pyrethroids with organophosphorus and carbamate insecticides applied to western spruce budworm (Lepidoptera: Tortricidae). Journal of Economic Entomology, 77: 16–22.CrossRefGoogle Scholar
Robertson, J.L., Russell, R.M., Preisler, H., and Savin, N.E. 2007. Bioassays with arthropods. CRC Press, Taylor and Francis Group, New York.CrossRefGoogle Scholar
Rosengren, K.J., Wilson, D., Daly, N.L., Allewood, P.F., and Craik, D.J. 2002. Solution structures of the cis- and trans-Pro30 isomers of a novel 38-residue toxin from the venom of Hadronyche infensa sp. that contains a cystineknot motif within its four disulfide bonds. Biochemistry, 41: 3294–3301. PMID:11876637 doi:10.1021/bi011932y.CrossRefGoogle ScholarPubMed
Saxena, R.C., Jilani, G., and Abdul-Kareem, A. 1988. Effects of neem on stored grain insects. In Focus on phytochemical pesticides. Vol. 1. The neem tree. Edited by Jacobson, J.. CRC Press Inc., Boca Raton, Florida. pp. 97–111.Google Scholar
Schöller, M., and Flinn, P.W. 2000. Parasites and predators. In Alternatives to pesticides in stored-product IPM. Edited by Subramanyam, B. and Hagstrum, D., Kluwer Academic Publishers, London, United Kingdom. pp. 303–320.Google Scholar
Shimoyamada, M., Ikedo, S., Ootsubo, R., and Watanabe, K. 1998. Effects of soybean saponins on chymotryptic hydrolases of soybean proteins. Journal of Agricultural and Food Chemistry, 46: 4793–4797. doi:10.1021/jf980694j.CrossRefGoogle Scholar
Silcox, C., and Roth, E. 1995. Pyrethrum for control of pests of agricultural and stored products. In Pyrethrum flowers: production, chemistry, toxicology, and uses. Edited by Casida, J.E. and Quistad, G.B.. Oxford University Press, New York. pp. 287–301.Google Scholar
Snelson, J.T. 1987. Grain protectants. Australian Centre for International Agricultural Research, Canberra, Australia.Google Scholar
Sokal, R.R., and Rohlf, F.J. 1981. Biometry. W.H. Freeman and Co., San Francisco.Google Scholar
SPSS Inc. 2003. SigmaStat version 3.0. User's guide. SPSS Inc., Chicago.Google Scholar
Subramanyam, B., and Hagstrum, D. 1995. Resistance measurement and management. In Integrated management of insects in stored products. Edited by Subramanyam, B. and Hagstrum, D.. Marcel Dekker Inc., New York. pp. 331–398.Google Scholar
Subramanyam, B., and Hagstrum, D. 2000. Alternatives to pesticides in stored-product IPM. Kluwer Academic Publishers, London, United Kingdom.CrossRefGoogle Scholar
Sun, Y.P., and Johnson, E.R. 1960. Analysis of joint action of insecticides against house flies. Journal of Economical Entomology, 53: 887–892.CrossRefGoogle Scholar
Taylor, W.G., Fields, P.G., and Elder, J.L. 2004 a. Insecticidal components from field pea extracts: isolation and separation of peptide mixtures related to pea albumin 1b. Journal of Agricultural and Food Chemistry, 52: 7491–7498. PMID:15675794 doi:10.1021/jf030806t.CrossRefGoogle ScholarPubMed
Taylor, W.G., Fields, P.G., and Sutherland, D.H. 2004 b. Insecticidal components from field pea extracts: soyasaponins and lysolecithins. Journal of Agricultural and Food Chemistry, 52: 7484–7490. PMID:15675793 doi:10.1021/jf0308051.CrossRefGoogle ScholarPubMed
Taylor, W.G., Sutherland, D.H., Olson, D.J.H., Ross, A.R.S., and Fields, P.G.. 2004 c. Insecticidal components from field pea extracts: sequences of some variants of pea albumin 1b. Journal of Agricultural and Food Chemistry, 52: 7499–7506. PMID:15675795 doi:10.1021/jf030807l.CrossRefGoogle ScholarPubMed
Taylor, W.G., Fields, P.G., and Sutherland, D.H. 2007. Fractionation of lentil seeds (Lens culinaris Medik.) for insecticidal and flavonol tetraglycoside components. Journal of Agricultural and Food Chemistry, 55: 5491–5498. PMID:17567145 doi:10.1021/jf0705062.CrossRefGoogle ScholarPubMed
United States Environmental Protection Agency. 2010. Expanding use restrictions to reduce risks of aluminum and magnesium phosphide [online]. Available from http://www.epa.gov/oppsrrd1/reregistration/alphosphide/aluminum-magnsm-phos-fs.html#expanded [accessed 26 April 2010].Google Scholar
Waligora, D. 1998. Biological activity of secondary plant substances glucosinolates, alkaloids and saponins, expressed by their effects on development of Colorado potato beetle, Leptinotarsa decemlineata Say. Journal of Plant Protection Research, 38: 158–173.Google Scholar
Wawrzyniak, M., Blazejewska, A., and Jurzysta, M. 2003. Effect of alfalfa (Medicago sativa L.) saponins on development and fertility of grain weevil (Sitophilus granarius L.). Acta Scientiarum Polonorum Agricultura, 2: 119–124.Google Scholar
Weaver, D., and Subramanyam, B. 2000. Botanicals. In Alternatives to pesticides in stored-product IPM. Edited by Subramanyam, B. and Hagstrum, D.. Kluwer Academic Publishers, London, United Kingdom. pp. 303–320.CrossRefGoogle Scholar
Xia, C., Yang, Z., Zhu, B., and Yong, Y. 2000. Progress on the research field of tea saponin application in pesticide industry. Journal of Tea Science, 20: 82–88.Google Scholar
Xie, Y.S., Fields, P.G., and Isman, M.B. 1995. Repellency and toxicity of azadirachtin and neem to three stored-product insects. Journal of Economical Entomology, 88: 1024–1031.CrossRefGoogle Scholar
Xie, Y.S., Bodnaryk, R.P., and Fields, P.G. 1996. A rapid and simple flour disk bioassay for testing substances active against stored-product insects. The Canadian Entomologist, 128: 865–875. doi: 10.4039/Ent128865-5CrossRefGoogle Scholar