Stilbenes from grapevine root: a promising natural insecticide against Leptinotarsa decemlineata

Abstract

Stilbenes are phenolic compounds which are produced in large amounts in vine and are involved in plant defence as phytoalexins. Oligomeric forms have recently proven to be the most active compounds against a wide range of parasites such as fungi, bacteria or algae. The aim of this study was to investigate the activity of a grapevine root extract which is a stilbene oligomer pool against Leptinotarsa decemlineata, a major pest of Solanaceae crops. Analysis by UHPLC-DAD-MS of the stilbene-enriched extract obtained from grapevine root (Riparia Gloire de Montpellier rootstock) highlighted twelve stilbenes at 25% (w/w). The major stilbenes found in root extract were isolated such as the tetramers vitisin B, vitisin A and hopeaphenol; the dimers ampelopsin A and E-ε-viniferin and the monomer E-resveratrol. The insecticidal effects of this extract as well as the main compounds were investigated against L. decemlineata larvae. The extract caused chronic toxicity, inhibited larval development and, to a lesser extent, inhibited food intake. The high concentrations of vitisin A and vitisin B in grapevine root contributed to this effect as they are the most toxic compounds. Outdoor pot experiments revealed the efficacy of stilbene-enriched extract with high mortality of L. decemlineata and protection of potato plants. The extract also revealed an absence of toxicity against non-targeted organisms such as earthworms (Eisenia fetida). Thus, these results strongly suggest that grapevine roots are a promising source of bioactive stilbenes for the development of natural insecticides.

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References

  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    CAS  Article  Google Scholar 

  2. Ali A, Strommer J (2003) A simple extraction and chromatographic system for the simultaneous analysis of anthocyanins and stilbenes of Vitis species. J Agric Food Chem 51:7246–7251. https://doi.org/10.1021/jf030435g

    CAS  Article  PubMed  Google Scholar 

  3. Alyokhin A, Baker M, Mota-Sanchez D, Dively G, Grafius E (2008) Colorado potato beetle resistance to insecticides. Am J Potato Res 85:395–413. https://doi.org/10.1007/s12230-008-9052-0

    Article  Google Scholar 

  4. Finney DJ (1971) Probit analysis. Cambridge University Press, London

    Google Scholar 

  5. Flamini R, De Rosso M, De Marchi F, Dalla Vedova A, Panighel A, Gardiman M, Maoz I, Bavaresco L (2013) An innovative approach to grape metabolomics: stilbene profiling by suspect screening analysis. Metabolomics. https://doi.org/10.1007/s11306-013-0530-0

    Google Scholar 

  6. FranceAgriMer (2012) L’observatoire national des ressources en biomasse. Évaluation des ressources disponibles en France. http://www.franceagrimer.fr/Stockage-Actualites/Archives/2012/Observatoire-national-des-ressources-en-biomasse-evaluation-desressources

  7. Gabaston J, Cantos-Villar E, Biais B, Waffo-Teguo P, Renouf E, Corio-Costet MF, Richard T, Mérillon JM (2017) Stilbenes from Vitis vinifera L. waste: a sustainable tool for controlling Plasmopara Viticola. J Agric Food Chem 65:2711–2718. https://doi.org/10.1021/acs.jafc.7b00241

    CAS  Article  PubMed  Google Scholar 

  8. Giovinazzo G, Grieco F (2015) Functional properties of grape and wine polyphenols. Plant Foods Hum Nutr 70:454–462. https://doi.org/10.1007/s11130-015-0518-1

    CAS  Article  PubMed  Google Scholar 

  9. Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, Hoboken

    Google Scholar 

  10. González-Sarrías A, Gromek S, Niesen D, Seeram NP, Henry GE (2011) Resveratrol oligomers isolated from Carex species inhibit growth of human colon tumorigenic cells Mediated by Cell Cycle Arrest. J Agric Food Chem 59:8632–8638. https://doi.org/10.1021/jf201561e

    Article  PubMed  Google Scholar 

  11. Guerrero RF, Biais B, Richard T, Puertas B, Waffo-Teguo P, Merillon JM, Cantos-Villar E (2016) Grapevine cane’s waste is a source of bioactive stilbenes. Ind Crops Prod 94:884–892. https://doi.org/10.1016/j.indcrop.2016.09.055

    CAS  Article  Google Scholar 

  12. Harmatha J, Dinan L (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interactions. Phytochem Rev 2:321–330. https://doi.org/10.1023/b:phyt.0000045494.98645.a3

    CAS  Article  Google Scholar 

  13. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Tree 15:238–243. https://doi.org/10.1016/S0169-5347(00)01861-9

    PubMed  Google Scholar 

  14. Isman MB (2015) A renaissance for botanical insecticides: a renaissance for botanical insecticides. Pest Manag Sci 71:1587–1590. https://doi.org/10.1002/ps.4088

    CAS  Article  PubMed  Google Scholar 

  15. Korhammer S, Reniero F, Mattivi F (1995) An oligostilbene from Vitis roots. Phytochemistry 38:1501–1504. https://doi.org/10.1016/0031-9422(94)00811-7

    CAS  Article  Google Scholar 

  16. Kuiters AT (1990) Role of phenolic substances from decomposing forest litter in plant-soil interactions. Acta Bot Neerlandica 39:329–348

    CAS  Article  Google Scholar 

  17. Lambert C, Bisson J, Waffo-Téguo P, Papastamoulis Y, Richard T, Corio-Costet MF, Mérillon JM, Cluzet S (2012) Phenolics and their antifungal role in grapevine wood decay: focus on the Botryosphaeriaceae family. J Agric Food Chem 60:11859–11868. https://doi.org/10.1021/jf303290g

    CAS  Article  PubMed  Google Scholar 

  18. Lambert C, Richard T, Renouf E, Bisson J, Waffo-Téguo P, Bordenave L, Ollat N, Mérillon JM, Cluzet S (2013) Comparative analyses of stilbenoids in canes of major Vitis vinifera L. cultivars. J Agric Food Chem 61:11392–11399. https://doi.org/10.1021/jf403716y

    CAS  Article  PubMed  Google Scholar 

  19. Leake JR, Rend DJ (1989) The effects of phenolic compounds on nitrogen mobilisation by ericoid mycorrhizal systems. Agric Ecosyst Environ 29:225–236. https://doi.org/10.1016/0167-8809(90)90281-h

    Article  Google Scholar 

  20. Liu YQ, Li XJ, Zhao CY, Lu Y, Li WQ, Liu ZL, Feng G, Yang L (2013) Synthesis and insect antifeedant activity of stilbene derivatives against Brontispa longissima larvae. Med Chem Res 22:2196–2206. https://doi.org/10.1007/s00044-012-0212-x

    CAS  Article  Google Scholar 

  21. Lv XQ, Feng G, Liu YQ, Nan X, Yang L (2014) CA-4, a natural cis-stilbene compound with potential insecticidal activity. Med Chem Res 23:3347–3352. https://doi.org/10.1007/s00044-014-0917-0

    CAS  Article  Google Scholar 

  22. Mattivi F, Vrhovsek U, Malacarne G, Masuero D, Zulini L, Stefanini M, Moser C, Velasco R, Guella G (2011) Profiling of resveratrol oligomers, important stress metabolites, accumulating in the leaves of hybrid Vitis vinifera (Merzling × Teroldego) genotypes infected with Plasmopara viticola. J Agric Food Chem 59:5364–5375. https://doi.org/10.1021/jf200771y

    CAS  Article  PubMed  Google Scholar 

  23. OECD (1984) OECD Guideline for testing of chemicals: earthworm, acute toxicity tests, vol 207. OECD, Paris

    Google Scholar 

  24. Oshima Y, Kamijou A, Ohizumi Y, Niwa M, Ito J, Hisamichi K, Takeshita M (1995) Novel oligostilbenes from Vitis coignetiae. Tetrahedron 51:11979–11986. https://doi.org/10.1016/0040-4020(95)00757-y

    CAS  Article  Google Scholar 

  25. Pavela R (2010) Antifeedant activity of plant extracts on Leptinotarsa decemlineata Say. and Spodoptera littoralis Bois. larvae. Ind Crops Prod 32:213–219. https://doi.org/10.1016/j.indcrop.2010.04.010

    Article  Google Scholar 

  26. Pavela R (2011) Antifeedant and larvicidal effects of some phenolic components of essential oils lasp lines of introduction against Spodoptera littoralis (Boisd.). J Essent Oil Bear Plants 14:266–273. https://doi.org/10.1080/0972060X.2011.10643932

    CAS  Article  Google Scholar 

  27. 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 Prot Sci 52:229–241. https://doi.org/10.17221/31/2016-PPS

    Article  Google Scholar 

  28. Pavela R, Vrchotová N, Šerá B (2008) Growth inhibitory effect of extracts from Reynoutria sp. plants against Spodoptera littoralis larvae. Agrociencia 42:573–584 (ISSN 1405-3195)

    Google Scholar 

  29. Pavela R, Waffo-Teguo P, Biais B, Richard T, Mérillon JM (2017) Vitis vinifera canes, a source of stilbenoids against Spodoptera littoralis larvae. J Pest Sci 90:961–970. https://doi.org/10.1007/s10340-017-0836-1

    Article  Google Scholar 

  30. Pawlus AD, Waffo-Teguo P, Shaver J, Merillon JM (2012) Stilbenoid chemistry from wine and the genus Vitis, a review. J Int Sci Vigne Vin 46:57–111

    CAS  Google Scholar 

  31. Renaud S, De Lorgeril M (1992) Wine alcohol, platelets, and the French paradox for coronary heart disease. Prentice Hall, Englewood Cliffs, NJ, Prentice Hall endocrinology series. https://doi.org/10.1016/0140-6736(92)91277-f

    Google Scholar 

  32. Richard T, Poupard P, Nassra M, Papastamoulis Y, Iglésias ML, Krisa S, Waffo-Teguo P, Mérillon JM, Monti JP (2011) Protective effect of ε-viniferin on β-amyloid peptide aggregation investigated by electrospray ionization mass spectrometry. Bioorg Med Chem 19:3152–3155. https://doi.org/10.1016/j.bmc.2011.04.001

    CAS  Article  PubMed  Google Scholar 

  33. Rivière C, Pawlus AD, Mérillon JM (2012) Natural stilbenoids: distribution in the plant kingdom and chemotaxonomic interest in Vitaceae. Nat Prod Rep 29:1317. https://doi.org/10.1039/c2np20049j

    Article  PubMed  Google Scholar 

  34. Sambangi P, Rani PU (2016) Physiological effects of resveratrol and coumaric acid on two major groundnut pests and their egg parasitoid behavior: effect of phenolics on S. litura and A. albistriga. Arch Insect Biochem Physiol 91:230–245. https://doi.org/10.1002/arch.21320

    CAS  Article  PubMed  Google Scholar 

  35. Schnee S, Queiroz EF, Voinesco F, Marcourt L, Dubuis PH, Wolfender JL, Gindro K (2013) Vitis vinifera Canes, a new source of antifungal compounds against Plasmopara viticola, Erysiphe necator, and Botrytis cinerea. J Agric Food Chem 61:5459–5467. https://doi.org/10.1021/jf4010252

    CAS  Article  PubMed  Google Scholar 

  36. Shimizu K, Kondo R, Sakai K (2000) Inhibition of tyrosinase by flavonoids, stilbenes and related 4-substituted resorcinols: structure-activity investigations. Planta Med 66:11–15. https://doi.org/10.1055/s-2000-11113

    CAS  Article  PubMed  Google Scholar 

  37. Soeur J, Eilstein J, Léreaux G, Jones C, Marrot L (2015) Skin resistance to oxidative stress induced by resveratrol: from Nrf2 activation to GSH biosynthesis. Free Radic Biol Med 78:213–223. https://doi.org/10.1016/j.freeradbiomed.2014.10.510

    CAS  Article  PubMed  Google Scholar 

  38. Stoytcheva M (2011) Pesticides in the modern world: effects of pesticides exposure. Intech, Croatia

    Google Scholar 

  39. Torres P, Guillermo Avila J, Romo de Vivar A, Garcı́a AM, Marı́n JC, Aranda E, Céspedes CL (2003) Antioxidant and insect growth regulatory activities of stilbenes and extracts from Yucca periculosa. Phytochemistry 64:463–473. https://doi.org/10.1016/S0031-9422(03)00348-0

    CAS  Article  PubMed  Google Scholar 

  40. Vitrac X, Bornet A, Vanderlinde R, Valls J, Richard T, Delaunay JC, Mérillon JM, Teissédre PL (2005) Determination of stilbenes (δ-viniferin, trans-astringin, trans-piceid, cis- and trans-resveratrol, ε-viniferin) in Brazilian wines. J Agric Food Chem 53:5664–5669. https://doi.org/10.1021/jf050122g

    CAS  Article  PubMed  Google Scholar 

  41. Xia EQ, Deng GF, Guo YJ, Li HB (2010) Biological activities of polyphenols from grapes. Int J Mol Sci 11:622–646. https://doi.org/10.3390/ijms11020622

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Dr. Pavela would like to thank the Ministry of Agriculture in the Czech Republic for financial support of botanical pesticide and basic substance research. Financial support for this work was provided by Project No. QJ1610082.

Funding

The authors also wish to thank the Conseil Regional d’Aquitaine for their financial support in this research. The work was supported by the Bordeaux Metabolome Facility and MetaboHUB (ANR-11-INBS-0010 Project).

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RP, PWT and JMM conceived the project. JG, TK, TR, AD and RP performed the experiments. JG, JMM and RP wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Jean-Michel Mérillon.

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

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Communicated by M.B. Isman.

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Gabaston, J., El Khawand, T., Waffo-Teguo, P. et al. Stilbenes from grapevine root: a promising natural insecticide against Leptinotarsa decemlineata. J Pest Sci 91, 897–906 (2018). https://doi.org/10.1007/s10340-018-0956-2

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Keywords

  • Botanical insecticide
  • Solanaceae
  • Colorado potato beetle
  • Vine root extract
  • Stilbene
  • Vitisins