Abstract
Enhancing natural mechanisms of plant defense against herbivores is one of the possible strategies to protect cultivated species against insect pests. Host plant feeding stimulation, which results from phagostimulant and phagodeterrent effects of both primary and secondary metabolites, could play a key role in levels of damage caused to crop plants. We tested this hypothesis by comparing the feeding intensity of the pollen beetle Meligethes aeneus on six oilseed rape (Brassica napus) genotypes in a feeding experiment, and by assessing the content of possible phagostimulant and phagodeterrent compounds in tissues targeted by the insect (flower buds). For this purpose, several dozens of primary and secondary metabolites were quantified by a set of chromatographic techniques. Intergenotypic variability was found both in the feeding experiment and in the metabolic profile of plant tissues. Biochemical composition of the perianth was in particular highly correlated with insect damage. Only a few compounds explained this correlation, among which was sucrose, known to be highly phagostimulating. Further testing is needed to validate the suggested impact of the specific compounds we have identified. Nevertheless, our results open the way for a crop protection strategy based on artificial selection of key determinants of insect feeding stimulation.
Similar content being viewed by others
References
Adams MA, Chen ZL, Landman P, Colmer TD (1999) Simultaneous determination by capillary gas chromatography of organic acids, sugars, and sugar alcohols in plant tissue extracts as their trimethylsilyl derivatives. Anal Biochem 266:77–84
Alagar M, Suresh S, Samiyappan R, Saravanakumar D (2007) Reaction of resistant and susceptible rice genotypes against brown planthopper (Nilaparvata lugens). Phytoparasitica 35:346–356
Ali K, Maltese F, Zyprian E, Rex M, Choi YH, Verpoorte R (2009) NMR metabolic fingerprinting based identification of grapevine metabolites associated with downy mildew resistance. J Agric Food Chem 57:9599–9606
Barker M, Rayens W (2003) Partial least squares for discrimination. J Chemometr 17:166–173
Barrett RD, Agrawal AA (2004) Interactive effects of genotype, environment, and ontogeny on resistance of cucumber (Cucumis sativus) to the generalist herbivore Spodoptera exigua. J Chem Ecol 30:37–54
Bartlet E, Williams IH (1991) Factors restricting the feeding of the cabbage stem flea beetle (Psylliodes chrysocephala). Entomol Exp Appl 60:233–238
Bartlet E, Parsons D, Williams IH, Clark SJ (1994) The influence of glucosinolates and sugars on feeding by the cabbage stem flea beetle, Psylliodes chrysocephala. Entomol Exp Appl 73(1):77–83
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300
Berenbaum MR (1995) Turnabout is fair play: secondary roles for primary compounds. J Chem Ecol 21:925–940
Berenbaum MR, Zangerl AR (2008) Facing the future of plant-insect interaction research: le retour à la “raison d’être”. Plant Physiol 146:804–811
Blight MM, Smart LE (1999) Influence of visual cues and isothiocyanates lures on capture of the pollen beetle, Meligethes aeneus in field traps. J Chem Ecol 25:1501–1516
Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367
Carrié RJ, George DR, Wäckers FL (2012) Selection of floral resources to optimize conservation of agriculturally-functional insect groups. J Insect Conserv 16:635–640
Chapman RF (2003) Contact chemoreception in feeding by phytophagous insects. Annu Rev Entomol 48:455–484
Charpentier R (1985) Host plant selection by the pollen beetle Meligethes aeneus. Entomol Exp Appl 38:277–285
Clissold FJ, Sanson GD, Read J, Simpson SJ (2009) Gross vs. net income : how plant toughness affects performance of an insect herbivore. Ecology 90(12):3393–3405
Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol Entomol 28:622–627
Cook SM, Smart LE, Martin JL, Murray DA, Watts NP, Williams IH (2006) Exploitation of host plant preferences in pest management strategies for oilseed rape (Brassica napus). Entomol Exp Appl 119:221–229
Cook SM, Rasmussen HB, Birkett MA, Murray DA, Pye BJ, Watts NP, Williams IH (2007) Behavioural and chemical ecology underlying the success of turnip rape (Brassica rapa) trap crops in protecting oilseed rape (Brassica napus) from the pollen beetle (Meligethes aeneus). Arthropod Plant Interact 1:57–67
Després L, David JP, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307
Diaz Napal GN, Carpinella MC, Palacios SM (2009) Antifeedant activity of ethanolic extract from Flourensia oolepis and isolation of pinocembrin as its active principle compound. Bioresour Technol 100:3669–3673
Diaz Napal GN, Defagó MT, Valladares GR, Palacios MT (2010) Response of Epilachna paenulata to two flavonoids, pinocembrin and quercetin, in a comparative study. J Chem Ecol 36:898–904
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Eickermann M, Ulber B (2010) Screening of oilseed rape and other brassicaceous genotypes for susceptibility to Ceutorhynchus pallidactylus (Mrsh.). J Appl Entomol 134:542–550
Ekbom B, Borg A (1996) Pollen beetle (Meligethes aeneus) oviposition and feeding preference on different host plant species. Entomol Exp Appl 78:291–299
El Bouhssini M, Ogbonnaya FC, Chen M, Lhaloui S, Rihawi F, Dabbous A (2013) Sources of resistance in primary synthetic hexaploid wheat (Triticum aestivum L.) to insect pests: Hessian fly, Russian wheat aphid and Sunn pest in the fertile crescent. Genet Resour Crop Evol 60:621–627
Francisco M, Moreno DA, Cartea ME, Ferreres F, Farciá-Viguera C, Velasco P (2009) Simultaneous identification of glucosinolates and phenolics compounds in a representative collection of vegetable Brassica rapa. J Chromatogr A 1216:6611–6619
Free JB, Williams IH (1978) The responses of the pollen beetle, Meligethes aeneus, and the seed weevil, Ceutorhynchus assimilis, to oil-seed rape, Brassica napus, and other plants. J Appl Ecol 15:761–774
Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156:145–169
Giamoustaris A, Mithen R (1995) The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests. Ann Appl Biol 126:347–363
Glynn C, Rönnberg-Wästljung AC, Julkunen-Tiitto R, Weih M (2004) Willow genotype, but not drought treatment, affects foliar phenolics concentrations and leaf-beetle resistance. Entomol Exp Appl 113:1–14
González I, Lé Cao KA, Déjean S (2011) mixOmics: omics data integration project. URL: http://www.math.univ-toulouse.fr/~biostat/mixOmics/
Gravot A, Dittami SM, Rousvoal S, Lugan R, Eggert A, Collén J, Boyen C, Bouchereau A, Tonon T (2010) Diurnal oscillations of metabolite abundances and gene analysis provide new insights into central metabolic processes of the brown alga Ectocarpus siliculosus. New Phytol 188:98–110
Gruber MY, Wang S, Ethier S, Holowachuk J, Bonham-Smith PC, Soroka J, Lloyd A (2006) “Hairy canola”—Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol Biol 60:679–698
Henery ML, Henson M, Wallis IR, Stone C, Foley WJ (2008) Predicting crown damage to Eucalyptus grandis by Paropsis atomaria with direct and indirect measures of leaf composition. For Ecol Manag 255:3642–3651
Hollister B, Mullin CA (1998) Behavioral and electrophysiological dose–response relationships in adult western corn rootworm (Diabrotica virgifera virgifera LeConte) for host pollen amino acids. J Insect Physiol 44:463–470
Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83
Hori M, Nakamura H, Fujii Y, Suzuki Y, Matsuda K (2010) Chemicals affecting the feeding preference of the Solanaceae-feeding lady beetle Henosepilachna vigintioctomaculata (Coleoptera: Coccinellidae). J Appl Entomol 135:121–161
Isidoro N, Bartlet E, Ziesmann J, Williams IH (1998) Antennal contact chemosensilla in Psylliodes chrysocephala responding to cruciferous allelochemicals. Physiol Entomol 23:131–138
Jackson DM, Harrison HF (2013) Insect resistance in traditional and heirloom sweetpotato varieties. J Econ Entomol 106:1456–1462
Jubault M, Hamon C, Gravot A, Lariagon C, Delourme R, Bouchereau A, Manzanares-Dauleux MJ (2008) Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol 146:2008–2019
Kim JH, Mullin CA (1998) Structure-phagostimulatory relationships for amino acids in adult western corn rootworm, Diabrotica virgifera virgifera. J Chem Ecol 24:1499–1511
Knutson AE, Mekala KD, Smith CW, Campos C (2013) Tolerance to feeding damage by cotton fleahopper (Hemiptera: Miridae) among genotypes representing adapted germplasm pools of United States upland cotton. J Econ Entomol 106:1045–1052
Kühnle A, Müller C (2009) Differing acceptance of familiar and unfamiliar plant species by an oligophagous beetle. Entomol Exp Appl 131:189–199
Lancashire PD, Bleiholder H, Vandenboom T, Langeluddeke P, Strauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth-stages of crops and weeds. Ann Appl Biol 119:561–601
Leiss KA, Cristofori G, van Steenis R, Verpoorte R, Klinkhamer PG (2013) An eco-metabolomic study of host plant resistance to western flower thrips in cultivated, biofortified and wild carrots. Phytochemistry 93:63–70
Lenth RV (2013) lsmeans: Least-squares means. R package version 1.10–4. http://CRAN.R-project.org/package=lsmeans
Lin S, Mullin CA (1999) Lipid, polyamide, and flavonols phagostimulants for adult western corn rootworm from sunflower (Helianthus annuus L.) pollen. J Agric Food Chem 47:1223–1229
Lugan R, Niogret MF, Kervazo L, Larher FR, Kopka J, Bouchereau A (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant Cell Environ 32:95–108
Lyytinen A, Lindström L, Mappes J, Julkunen-Tiitto R, Fasulati S, Tiilikkala K (2007) Variability in host plant chemistry: behavioural responses and life-history parameters of the Colorado potato beetle (Leptinotarsa decemlineata). Chemoecology 17:51–56
Marques I, Draper D (2012) Pollination activity affects selection on floral longevity in the autumnal-flowering plant, Narcissus serotinus L. Botany 90:283–291
Merivee E, Märtmann H, Must A, Milius M, Williams IH, Mänd M (2008) Electrophysiological responses from neurons of antennal taste sensilla in the polyphagous predatory ground beetle Pterostichus oblongopunctatus (Fabricius 1787) to plant sugars and amino acids. J Insect Physiol 54:1213–1219
Merivee E, Must A, Tooming E, Williams IH, Sibul I (2012) Sensitivity of antennal gustatory receptor neurons to aphid honeydew sugars in the carabid Anchomenus dorsalis. Physiol Entomol 37:369–378
Mitchell BK, Gregory P (1979) Physiology of the maxillary sugar sensitive cell in the red turnip beetle, Entomoscelis Americana. J Comp Physiol A 132:167–178
Mitchell BK, Schoonhoven LM (1974) Taste receptors in Colorado beetle larvae. J Insect Physiol 20:1787–1793
Nielsen JK, Larsen LM, Sørensen H (1979) Host plant selection of the horseradish flea beetle Phyllotreta armoraciae (Coleoptera: Chrysomelidae): identification of two flavonols glycosides stimulating feeding in combination with glucosinolates. Entomol Exp Appl 26:40–48
Nilsson C (1988) The pollen beetle (M. aeneus F.) in winter and spring rape at Alnarp 1976–1978. II. Oviposition. Vaxtskyddsnotiser 52:139–144
Niveyro SL, Mortensen AG, Fomsgaard IS, Salvo A (2013) Differences among five amaranth varieties (Amaranthus spp.) regarding secondary metabolites and foliar herbivory by chewing insects in the field. Arthropod Plant Interact 7:235–245
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Rapacz M (1998) Physiological effects of winter rape (Brassica napus var. oleifera) prehardening to frost. II. Growth, energy partitioning and water status during cold acclimation. J Agron Crop Sci 181:81–87
Ruther J, Thiemann K (1997) Response of the pollen beetle Meligethes aeneus to volatiles emitted by intact plants and conspecifics. Entomol Exp Appl 84:183–188
Sasaki H, Ichimura K, Oda M (1996) Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Ann Bot 78:365–369
Simmonds MS (2001) Importance of Flavonoids in insect-plant interactions: feeding and oviposition. Phytochemistry 56:245–252
Simmonds MS (2003) Flavonoid-insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30
Smart LE, Blight MM (2000) Response of the pollen beetle, Meligethes aeneus, to traps baited with volatiles from oilseed rape, Brassica napus. J Chem Ecol 26:1051–1064
Ströcker K, Wendt S, Kirchner WH, Struck C (2013) Feeding preferences of the weevils Sitona gressorius and Sitona griseus on different lupin genotypes and the role of alkaloids. Arthropod Plant Interact 7:579–589
Tefera T, Demissie G, Mugo S, Beyene Y (2013) Yield and agronomic performance of maize hybrids resistant to the maize weevil Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Crop Prot 46:94–99
Tooming E, Merivee E, Must A, Luik A, Williams IH (2012) Antennal sugar sensitivity in the click beetle Agriotes obscures. Physiol Entomol 37:345–353
Treutter D (2006) Significance of Flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157
Velasco P, Francisco M, Moreno DA, Ferreres F, García-Viguera C, Cartea ME (2011) Phytochemical fingerprinting of vegetable Brassica oleracea and Brassica napus by simultaneous identification of glucosinolates and phenolics. Phytochem Anal 22:144–152
Venables WN, Ripley BB (2002) Modern applied statistics with S, 4th edn. Springer, New York
Wagner G, Charton S, Lariagon C, Laperche A, Lugan R, Hopkins J, Frendo P, Bouchereau A, Delourme R, Gravot A, Manzanare-Dauleux MJ (2012) Metabotyping: a new approach to investigate rapeseed (Brassica napus L.) genetic diversity in the metabolic response to clubroot infection. Mol Plant Microbe In 25:1478–1491
Williams IH (2010) The major insect pests of oilseed rape in Europe and their management: an overview. In: Williams IH (ed) Biocontrol-based integrated management of oilseed rape pests. Springer, London, pp 1–43
Williams IH, Free JB (1978) The feeding and mating behaviour of pollen beetles (Meligethes aeneus Fab.) and seed weevils (Ceuthorhynchus assimilis Payk.) on oil-seed rape (Brassica napus L.). J Agric Sci 91:453–459
Acknowledgments
We are grateful to Sam Cook and Maria Manzanares-Dauleux for their very helpful comments on this study, to Mélanie Leclair, Céline Josso, Sonia Dourlot, Christine Lariagon, and Anne Boudier for technical help during the experiments, and to the UMR IGEPP glasshouse team for taking care of the plants used. Metabolic analyses were performed on the P2M2 platform (Le Rheu, France). Maxime Hervé was supported by a CJS grant from the French National Institute of Agronomical Research.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 26 kb)
Rights and permissions
About this article
Cite this article
Hervé, M.R., Delourme, R., Gravot, A. et al. Manipulating Feeding Stimulation to Protect Crops Against Insect Pests?. J Chem Ecol 40, 1220–1231 (2014). https://doi.org/10.1007/s10886-014-0517-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-014-0517-y