Abstract
Lignans and neolignans have been reported to exert different biological activities, including insecticidal ones. Three lignans, secoisolariciresinol (SECO), secoisolariciresinol diglucoside (SDG), and anhydrosecoisolariciresinol (AHS), and one neolignan, dehydrodiconiferyl alcohol-4-β-d-glucoside (DCG), were isolated from flax. Their insecticidal properties were evaluated on the aphid Myzus persicae reared on artificial diet. Life history parameters, i.e., nymphal survival, prereproductive period, and daily fecundity, were assessed and used to calculate the intrinsic rate of natural increase and the doubling time of aphid populations. Compared to the control, SDG and DCG significantly increased aphid mortality by at least 25 %, while SECO and AHS did not affect their survival. SDG did not affect life history parameters, except at the highest concentration of 100 μg/mL, which increased the population’s doubling time by more than 5 days. DCG altered all the life history parameters at all concentrations assayed. SECO induced significant deleterious effects on the aphids, except at the highest concentration of 100 μg/mL. AHS only altered prereproductive period, which increased by at least 2 days at 50 and 100 μg/mL. Lignans and neolignans are potential new bioinsecticides against aphids in the context of alternative management programs.
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References
Apers S, Vlietinck A, Pieters L (2003) Lignans and neolignans as lead compounds. Phytochem Rev 2:201–217
Attoumbré J, Charlet S, Baltora-Rosset S, Hano C, Raynaud-Le Grandic S, Gillet F, Bensaddek L, Mesnard F, Fliniaux MA (2006) High accumulation of dehydrodiconiferyl alcohol-4-β-d-glucoside in free and immobilized Linum usitatissimum cell cultures. Plant Cell Rep 25:859–864
Attoumbré J, Bienaimé C, Dubois F, Fliniaux MA, Chabbert B, Baltora-Rosset S (2010) Development of antibodies against secoisolariciresinol. Application to the immunolocalization of lignans in Linum usitatissimum seeds. Phytochemistry 71:1979–1987
Bernard CB, Arnason JT, Philogène BJR, Lam J, Waddell T (1989) Effect of lignans and other secondary metabolites of the asteraceae on the mono-oxygenase activity of the european corn borer. Phytochemistry 28(5):1373–1377
Blackman RL, Eastop VF (1984) Aphids on the world’s crops: an identification and information guide. John Wiley & Sons, Chichester
Bultel L, Saguez J, Giordanengo P, Kovensky J (2009) Compound of the disaccharide type composition comprising and method for producing such a compound. Patent WO2009098400 (A1)
Cabral MMO, Kelecom A, Garcia ES (1999) Effects of the lignan, pinoresinol on the moulting cycle of the bloodsucking bug Rhodnius prolixus and of the milkweed bug Oncopeltus fasciatus. Fitoterapia 70(6):561–567
Cabral MMO, Azambuja P, Gottlieb OR, Garcia ES (2000) Effects of some lignans and neolignans on the development and excretion of Rhodnius prolixus. Fitoterapia 71(1):1–9
Carlini CR, Grossi-de-Sá MF (2002) Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon 40(11):1515–1539
Cherqui A, Alla S, Saguez J, Doury G, Sangwan-Norreel BS, Giordanengo P (2003) Probiotic effects of beta-glucuronidase on the peach-potato aphid Myzus persicae (Aphididae). J Insect Physiol 49:1199–1209
Devonshire AL, Field LM, Foster SP, Moores GD, Williamson MS, Blackman RL (1998) The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philos Trans R Soc Lond B 353:1677–1684
Dixon RA (2004) Phytoestrogens. Annu Rev Plant Biol 55:225–261
Douglas AE (1992) Requirement of pea aphids (Acyrthosiphon pisum) for their symbiotic bacteria. Entomol Exp Appl 65:195–198
Down RE, Gatehouse AMR, Hamilton WDO, Gatehouse JA (1996) Snowdrop lectin inhibits development and decreases fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants both in laboratory and glasshouse trials. J Insect Physiol 42:1035–1045
Dussouy C, Bultel L, Saguez J, Cherqui A, Khelifa M, Grand E, Giordanengo P, Kovensky J (2012) Strong aphicidal activity of GlcNAc(β1-4)Glc disaccharides: synthesis, physiological effects and chitinase inhibition. Chem Eur J 18:10021–10028
Ferguson AW, Fitt BDL, Williams IH (1997) Insect injury to linseed in south-east England. Crop Prot 16(7):643–652
Flanders KL, Hawkes JG, Radcliffe EB, Lauer FI (1992) Insect resistance in potatoes: sources, evolutionary relationships, morphological and chemical defenses, and ecogeographical associations. Euphytica 61:83–111
Ford JD, Huang K-S, Wang H-B, Davin LB, Lewis NG (2001) Biosynthetic pathway to the cancer chemopreventive secoisolariciresinol diglucoside-hydroxymethyl glutaryl ester-linked lignan oligomers in flax (Linum usitatissimum) seed. J Nat Prod 64(11):1388–1397
Garcia ES, Azambuja P (2004) Lignoids in insects: chemical probes for the study of ecdysis, excretion and Trypanosoma cruzi-triatomine interactions. Toxicon 44:431–440
Giordanengo P (2012) DEMP 1.5.2, a php program to calculate demographic parameters (life table) INRA, Sophia Antipolis, France
Guntner C, Vazquez A, Gonzalez G, Usubillaga A, Ferreira F, Moyna P (2000) Effect of Solanum glycoalkaloids on potato aphid, Macrosiphum euphorbiae: part II. J Chem Ecol 26:1113–1121
Hano C, Martin I, Fliniaux O, Legrand B, Gutierrez L, Arroo R, Mesnard F, Lamblin F, Lainé E (2006) Pinoresinol–lariciresinol reductase gene expression and secoisolariciresinol diglucoside accumulation in developing flax (Linum usitatissimum) seeds. Planta 224(6):1291–1301
Harmatha J (2000) Chemo-ecological role of spirostanol saponins in the interaction between plant. In: Olezsek W, Marston A (eds) Saponins in food, feedstuffs and medicinal plants. Kluwer Academic Publishers, Dordrecht, pp 129–141
Harmatha J, Dinan L (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interaction. Phytochem Rev 2:321–330
Harmatha J, Nawrot J (2002) Insect feeding deterrent activity of lignans and related phenylpropanoids with a methylenedioxyphenyl (piperonyl) structure moiety. Entomol Exp Appl 104(1):51–60
Hullé M, Coeur d’Acier A, Bankhead-Dronnet S, Harrington R (2010) Aphids in the face of global changes. CR Biol 333:497–503
Jonasson T, Olsson K (1994) The influence of glycoalkaloids, chlorogenic acid and sugars on the susceptibility of potato to wireworm. Potato Res 37:205–216
Krajčová A, Schulzová V, Hajšlová J, Bjelková M (2009) Lignans in flaxseed. Czech J Food Sci 27:S252–S255
Lamb RJ, Grenkow L (2008) Efficiency of a herbivore-plant interaction: conversion of biomass from flax (Linaceae) to aphid, Macrosiphum euphorbiae (Hemiptera: Aphididae). Can Entomol 140:600–602
Le Roux V, Saguez J, Vincent C, Giordanengo P (2004) Rapid method to screen resistance of potato plants against Myzus persicae (Homoptera: Aphididae) in the laboratory. J Econ Entomol 97:2079–2082
Lehraiki A, Attoumbré J, Bienaimé C, Matifat F, Bensaddek L, Nava-Saucedo E, Fliniaux M-A, Ouadid-Ahidouch H, Baltora-Rosset S (2010) Extraction of lignans from flaxseed and evaluation of their biological effects on breast cancer MCF-7 and MDA-MB-231 cell lines. J Med Food 13:834–841
Li M, Han X, Yu B (2003) Synthesis of monomethylated dioscin derivatives and their antitumor activities. Carbohydr Res 338:117–121
Li W, Qiu Z, Wang Y, Zhang Y, Li M, Yu J, Zhang L, Zhu Z, Yu B (2007) Synthesis, cytotoxicity, and hemolytic activity of 6′-O-substituted dioscin derivatives. Carbohydr Res 342:2705–2715
MacRae WD, Towers GHN (1984) Biological activities of lignans. Phytochemistry 23:1207–1220
Messchendorp L, Gols GJZ, van Loon JJA (1998) Behavioral effects and sensory detection of drimane deterrents in Myzus persicae and Aphis gossypii nymphs. J Chem Ecol 24(9):1433–1446
Messiano GB, Vieira L, Machado MB, Lopes LMX, de Bortoli SA, Zukerman-Schpector J (2008) Evaluation of insecticidal activity of diterpenes and lignans from Aristolochia malmeana against Anticarsia gemmatalis. J Agric Food Chem 56(8):2655–2659
Moujir L, Seca AML, Silva AMS, Lopez MR, Padilla N, Cavaleiro JAS, Neto CP (2007) Cytotoxic activity of lignans from Hibiscus cannabinus. Fitoterapia 78:385–387
Nawrot J, Koul O, Isman MB, Harmatha J (1991) Naturally occurring antifeedants: effects on two polyphagous lepidopterans. J Appl Entomol 112(1–5):194–201
Pauletti PM, Araujo AR, Young MCM, Giesbrecht AM, Bolzani VS (2000) Nor-lignans from leaves of Styrax ferrugineus (Styracaceae) with antibacterial and antifungal activity. Phytochemistry 55:597–601
Pool-Zobel BL, Adlercreutz H, Glei M, Liegibel UM, Sittlington J, Rowland I, Wähälä K, Rechkemmer G (2000) Isoflavonoids and lignans have different potentials to modulate oxidative genetic damage in human colon cells. Carcinogenesis 21:1247–1252
Rayburn JR, Bantle JA, Friedman M (1994) Role of carbohydrate side chains of potato glycoalkaloids in developmental toxicity. J Agric Food Chem 42:1511–1515
Regnault-Roger C, Philogène BJR, Vincent C (2005) Biopesticides of plant origin. Intercept, Andover
Roddick JG, Weissenberg M, Leonard AL (2001) Membrane disruption and enzyme inhibition by naturally-occurring and modified chacotriose-containing Solanum steroidal glycoalkaloids. Phytochemistry 56:603–610
Russell GB, Pritam S, Fenemorec PG (1976) Insect-control chemicals from plants III. Toxic lignans from Libocedrus bidwillii. Aust J Biol Sci 29:99–104
Saguez J, Dubois F, Vincent C, Laberche J-C, Sangwan-Norreel B, Giordanengo P (2006) Differential aphicidal effects of chitinase inhibitors on the polyphagous homopteran Myzus persicae (Sulzer). Pest Manag Sci 62:1150–1154
Saguez J, Vincent C, Giordanengo P (2008) Chitinase inhibitors and chitin mimetics for crop protection. Pest Technol 2:81–86
Saleem M, Kim HJ, Ali MS, Lee YS (2005) An update on bioactive plant lignans. Nat Prod Rep 22:696–716
Sanford LL, Ladd TL (1992) Performance of populations derived by selecting for resistance to potato leafhopper in a 4XSolanum tuberosum X 2XSolanum chacoense cross. Am Potato J 69:391–400
Saraiva J, Vega C, Rolon M, da Silva R, Andrade e Silva ML, Donate PM, Bastos JK, Gomez-Barrio A, de Albuquerque S (2007) In vitro and in vivo activity of lignan lactones derivatives against Trypanosoma cruzi. Parasitol Res 100:791–795
Sasaki T, Hayashig G, Ishikawah H (1991) Growth and reproduction of the symbiotic and aposymbiotic pea aphids, Acyrthosiphon pisum, maintained on artificial diets. J Insect Physiol 37:749–756
Scott IM, Jensen HR, Philogene BJR, Arnason JT (2008) A review of Piper spp. (Piperaceae) phytochemistry, insecticidal activity and mode of action. Phytochem Rev 7:65–75
Sinden SL, Sanford LL, Osman SF (1980) Glycoalkaloids and resistance to the Colorado potato beetle in Solanum chacoense Bitter. Am Potato J 57:331–343
Sinden SL, Sanford LL, Cantelo WW, Deahl KL (1986) Leptine glycoalkaloids and resistance to the Colorado potato beetle (Coleoptera: Chrysomelidae) in Solanum chacoense. Environ Entomol 15:1057–1062
Sugahara T, Yamauchi S, Nishimoto S, Kondo A, Ohno F, Tominaga S, Nakashima Y, Kishida T, Akiyama K, Maruyama M, Kakinuma Y (2008) The structure-activity relationships of flaxseed lignan, secoisolariciresinol. In: Murakami Y, Nakayama K, Kitamura SI, Iwata H, Tanabe S (eds) Interdisciplinary studies on environmental chemistry—biological responses to chemical pollutants, vol 1. Terrapub, Tokyo, pp 263–268
Vargas-Arispuro I, Reyes-Baez R, Rivera-Castaneda G, Martinez-Téllez MA, Rivero-Espejel I (2005) Antifungal lignans from creosotebush (Larrea tridentate). Ind Crops Prod 22:101–107
Wilkinson TL, Douglas AE (1995) Why pea aphids (Acyrthosiphon pisum) lacking symbiotic bacteria have elevated levels of the amino acid glutamine. J Insect Physiol 41:921–927
Willför SM, Smeds AI, Holmbom BR (2006) Chromatographic analysis of lignans. J Chromatogr A 1112:64–77
Wise IL, Lamb RJ, Kenaschuk EO (1995) Effects of the potato aphid Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae) on oilseed flax, and stage-specific thresholds for control. Can Entomol 127:213–224
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The authors thank Charles Vincent and Noubar J Bostanian (Agriculture and Agri-Food Canada Saint-Jean-sur-Richelieu, Quebec) for their helpful advices and revisions on the manuscript and the “Centre de Valorisation des Glucides et des Produits Naturels” (Amiens, France) for providing L. usitatissimum seeds.
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Saguez, J., Attoumbré, J., Giordanengo, P. et al. Biological activities of lignans and neolignans on the aphid Myzus persicae (Sulzer). Arthropod-Plant Interactions 7, 225–233 (2013). https://doi.org/10.1007/s11829-012-9236-x
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DOI: https://doi.org/10.1007/s11829-012-9236-x