Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-08T15:26:22.788Z Has data issue: false hasContentIssue false

New insight into the behaviour modifying activity of two natural sesquiterpenoids farnesol and nerolidol towards Myzus persicae (Sulzer) (Homoptera: Aphididae)

Published online by Cambridge University Press:  27 September 2019

Anna Wróblewska-Kurdyk*
Affiliation:
Department of Botany and Ecology, University of Zielona Góra, Szafrana 1, 65-516Zielona Góra, Poland
Katarzyna Dancewicz
Affiliation:
Department of Botany and Ecology, University of Zielona Góra, Szafrana 1, 65-516Zielona Góra, Poland
Anna Gliszczyńska
Affiliation:
Department of Chemistry, Wrocław University of Environmental AND Life Sciences, Norwida 25, 50-375Wrocław, Poland
Beata Gabryś
Affiliation:
Department of Botany and Ecology, University of Zielona Góra, Szafrana 1, 65-516Zielona Góra, Poland
*
Author for correspondence: Anna Wróblewska-Kurdyk, Email: [email protected].

Abstract

The effect of structurally related sesquiterpenoids (E,E)-farnesol and cis-nerolidol on the host-plant selection behaviour of the peach potato aphid Myzus persicae (Sulz.) was evaluated using electrical penetration graph (EPG) technique. No repellent effects of (E,E)-farnesol and (Z)-nerolidol to M. persicae were found but aphid probing activities on (E,E)-farnesol- and cis-nerolidol-treated plants were restrained. During non-phloem phases of probing, neither (E,E)-farnesol nor (Z)-nerolidol affected the cell puncture activity. On (E,E)-farnesol-treated plants, the total duration of phloem phase, the mean duration of individual sustained ingestion periods were significantly lower, and the proportion of phloem salivation was higher than on control plants. On (Z)-nerolidol-treated plants, the occurrence of the first phloem phase was delayed, and the frequency of the phloem phase was lower than on control plants. The freely moving aphids were reluctant to remain on (E,E)-farnesol- and (Z)-nerolidol-treated leaves for at least 24 h after exposure. (E,E)-Farnesol and (Z)-nerolidol show complementary deterrent properties, (E,E)-farnesol showing ingestive and post-ingestive activities and nerolidol showing pre-ingestive, ingestive, and post-ingestive deterrent activities.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019

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

Abbas, F, Ke, Y, Yu, R, Yue, Y, Amanullah, S, Jahangir, MM and Fan, Y (2017) Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta 246, 803816.CrossRefGoogle ScholarPubMed
Aharoni, A, Jongsma, MA, Kim, T, Ri, M, Giri, AP, Verstappen, FWA, Schwab, W and Bouwmeester, HJ (2006) Metabolic engineering of terpenoid biosynthesis in plants. Phytochemistry Reviews 5, 4958.CrossRefGoogle Scholar
Alvarez, AE, Tjallingii, WF, Garzo, E, Vleeshouwers, V, Dicke, M and Vosman, B (2006) Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomologia Experimentalis et Applicata 121, 145157.CrossRefGoogle Scholar
Amaral, ACF, de Ramos, AS, Pena, MR, Ferreira, JLP, Menezes, JMS, Vasconcelos, GJN, da Silva, NM and de Andrade Silva, JR (2017) Acaricidal activity of Derris floribunda essential oil and its main constituent. Asian Pacific Journal of Tropical Biomedicine 7, 791796.CrossRefGoogle Scholar
Awad, HH and Ghazawy, NA (2016) Effects of farnesol on the ultrastructure of brain and corpora allata, sex hormones and on some oxidative stress parameters in Locusta migratoria (Orthoptera: Acrididae). African Entomology 24, 502513.CrossRefGoogle Scholar
Bass, C, Puinean, AM, Zimmer, CT, Denholm, I, Field, LM, Foster, SP, Gutbrod, O, Nauen, R, Slater, R and Williamson, MS (2014) The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology 51, 4151.CrossRefGoogle ScholarPubMed
Beer, K, Joschinski, J, Sastre, A, Krauss, J and Helfrich-Förster, C (2017) A damping circadian clock drives weak oscillations in metabolism and locomotor activity of aphids (Acyrthosiphon pisum). Scientific Reports 7, 14906.CrossRefGoogle Scholar
Bergman, P and Bergstrom, G (1997) Scent marking, scent origin, and species specificity in male premating behavior of two Scandinavian bumblebees. Journal of Chemical Ecology 23, 12351251.CrossRefGoogle Scholar
Blackman, R and Eastop, VF (2017) Taxonomic issues. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests. Wallingford, England: CABI. pp. 136.Google Scholar
Campos, EVR, Proençaa, PLF, Oliveiraa, JL, Bakshic, M, Abhilashc, PC and Fracetoa, LF (2019) Use of botanical insecticides for sustainable agriculture: future perspectives. Ecological Indicators 105, 483495.CrossRefGoogle Scholar
Cantrell, CL, Dayan, FE and Duke, SO (2012) Natural products as sources for new pesticides. Journal of Natural Products 75, 12311242.CrossRefGoogle ScholarPubMed
Chapman, RF and de Boer, G (1995) Regulatory mechanisms of insect feeding. In Chapman, RF and de Boer, G (eds), London: Chapman & Hall. pp. 1398.CrossRefGoogle Scholar
Chen, J, Martin, B, Raabe, Y and Fereres, A (1997) Early intracellular punctures by two aphid species on near-isogenic melon lines with and without the virus aphid transmission (Vat) resistance gene. European Journal of Plant Pathology 103, 521536.CrossRefGoogle Scholar
Culliney, TW (2014) Crop losses to arthropods. In Pimentel, D and Peshin, R (eds), Integrated Pest Management. Dordrecht: Springer Science + Business Media. pp. 201225.CrossRefGoogle Scholar
Dahlin, I, Vucetic, A and Ninkovic, V (2015) Changed host plant volatile emissions induced by chemical interaction between unattacked plants reduce aphid plant acceptance with intermorph variation. Journal of Pest Science 88, 249257.CrossRefGoogle Scholar
Dancewicz, K, Gabryś, B, Dams, I and Wawrzeńczyk, C (2008) Enantiospecific effect of pulegone and pulegone-derived lactones on settling and feeding of Myzus persicae (Sulz.). Journal of Chemical Ecology 34, 530538.CrossRefGoogle Scholar
Dancewicz, K, Gliszczyńska, A, Halarewicz, A, Wawrzeńczyk, C and Gabryś, B (2010) Effect of farnesol and its synthetic derivatives on the settling behaviour of the peach potato aphid Myzus persicae (Sulz.). Pesticides 1–4, 5157.Google Scholar
Dancewicz, K, Sznajder, K, Załuski, D, Kordan, B and Gabryś, B (2016) Behavioral sensitivity of Myzus persicae to volatile isoprenoids in plant tissues. Entomologia Experimentalis et Applicata 160, 229240.CrossRefGoogle Scholar
Gabryś, B and Pawluk, M (1999) Acceptability of different species of Brassicaceae as hosts for the cabbage aphid. Entomologia Experimentalis et Applicata 91, 105109.CrossRefGoogle Scholar
Gabryś, B, Dancewicz, K, Gliszczyńska, A, Kordan, B and Wawrzeńczyk, C (2015) Systemic deterrence of aphid probing and feeding by novel β-damascone analogues. Journal of Pest Science 88, 507516.CrossRefGoogle ScholarPubMed
Gerard, P, Perry, N, Ruf, L and Foster, L (1993) Antifeedant and insecticidal activity of compounds from Pseudowintera colorata (Winteraceae) on the webbing clothes moth, Tineola bisselliella (Lepidoptera: Tineidae) and the Australian carpet beetle, Anthrenocerus australis (Coleoptera: Dermestidae). Bulletin of Entomological Research 83, 547552.CrossRefGoogle Scholar
Goławska, S, Sprawka, I, Łukasik, I and Goławski, A (2014) Are naringenin and quercetin useful chemicals in pest-management strategies? Journal of Pest Science 87, 173180.CrossRefGoogle ScholarPubMed
Gonzalez-Coloma, A, Reina, M, Diaz, CE and Fraga, BM (2010) Natural product-based biopesticides for insect control. In Liu, HW and Mander, L (eds), Comprehensive Natural Products II. Chemistry and Biology, vol 3. Oxford, England: Elsevier. pp. 237268.Google Scholar
Gutierrez, C, Fereres, A, Reina, M, Cabrera, R and Gonzalez-Coloma, A (1997) Behavioral and sublethal effects of structurally related lower terpenes on Myzus persicae. Journal of Chemical Ecology 23, 16411650.CrossRefGoogle Scholar
Halarewicz, A and Gabryś, B (2012) Probing behavior of bird cherry-oat aphid Rhopalosiphum padi (L.) on native bird cherry Prunus padus L. and alien invasive black cherry Prunus serotina Erhr. in Europe and the role of cyanogenic glycosides. Arthropod-Plant Interactions 6, 497505.CrossRefGoogle Scholar
Halarewicz-Pacan, A, Gabryś, B, Dancewicz, K and Wawrzeńczyk, C (2003) Enantiospecific effect of limonene and limonene-derived bicyclic lactones on settling and probing behaviour of the peach-potato aphid Myzus persicae (Sulz.). Journal of Plant Protection Research 43, 133142.Google Scholar
Halbert, SE, Corsini, D and Vaughn, SF (2009) Plant derived compounds and extracts with potential as aphid repellents. Annals Applied Biology 154, 303307.CrossRefGoogle Scholar
Hardie, J, Holyoak, M, Taylor, NJ and Griffiths, DC (1992) The combination of electronic monitoring and video-assisted observations of plant penetration by aphids and behavioural effects of polygodial. Entomologia Experimentalis et Applicata 62, 233239.CrossRefGoogle Scholar
Harrewijn, P (1990) Resistance mechanisms of plant genotypes to various aphid species. In Campbell, RK and Eikenbary, RD (eds), Aphid-Plant Genotype Interactions. Amsterdam: Elsevier Science Publishers. pp. 117130.Google Scholar
Harrewijn, P, Oosten, AM and Piron, PGM (2001) Natural terpenoids as messengers. A multidisciplinary study of their production, biological functions and practical applications. In Harrewijn, P, Oosten, AM and Piron, PGM (eds), Dordrecht: Kluwer Academic Publishers. pp. 1424.Google Scholar
Hawkins, NJ, Bass, C, Dixon, A and Nevel, P (2019) The evolutionary origins of pesticide resistance. Biological Reviews 94, 135155.CrossRefGoogle Scholar
Isman, MB (2000) Plant essential oils for pest and disease management. Crop Protection 19, 603608.CrossRefGoogle Scholar
Isman, MB and Machial, CM (2006) Pesticides based on plant essential oils: from traditional practice to commercialization. In Rai, M and Carpinella, MC (eds), Naturally Occurring Bioactive Compounds. Amsterdam, Netherlands: Elsevier B.V. pp. 2944.CrossRefGoogle Scholar
Jackowski, J, Popłoński, J, Twardowska, K, Magiera-Dulewicz, J, Hurej, M and Huszcza, E (2017) Deterrent activity of hops flavonoids and their derivatives against stored product pests. Bulletin of Entomological Research 107, 592597.CrossRefGoogle ScholarPubMed
James, DG, Heffer, R and Amaike, M (1996) Field attraction of Biprorulus bibax Breddin (Hemiptera: Pentatomidae) to synthetic aggregation pheromone and (E)-2-hexenal, a pentatomid defense chemical. Journal of Chemical Ecology 22, 16971708.CrossRefGoogle Scholar
Jiang, Z, Kempinski, C and Chappell, J (2016) Extraction and analysis of terpenes/terpenoids. Current Protocols in Plant Biology 1, 345358.CrossRefGoogle ScholarPubMed
Joschinski, J, Beer, K, Helfrich-Forster, C and Krauss, J (2016) Pea aphids (Hemiptera: Aphididae) have diurnal rhythms when raised independently of a host plant. Journal of Insect Science 16, 31.CrossRefGoogle ScholarPubMed
Klein Gebbinck, EA, Jansen, BJM and de Groot, A (2002) Insect antifeedant activity of clerodane diterpenes and related model compounds. Phytochemistry 61, 737770.CrossRefGoogle ScholarPubMed
Knudsen, J, Eriksson, R, Gershenzon, J and Ståhl, B (2006) Diversity and distribution of floral scent. Botanical Review 72, 1120.CrossRefGoogle Scholar
Kordan, B, Dancewicz, K, Wróblewska, A and Gabryś, B (2012) Intraspecific variation in alkaloid profile of four lupine species with implications for the pea aphid probing behaviour. Phytochemistry Letters 5, 7177.CrossRefGoogle Scholar
Kordan, B, Stec, K, Słomiński, P, Laszczak-Dawid, A, Wróblewska-Kurdyk, A and Gabryś, B (2019) Antixenosis potential in pulses against the pea aphid (Hemiptera: Aphididae). Journal of Economic Entomology 112, 465474.CrossRefGoogle Scholar
Koul, O, Walia, S and Dhaliwal, GS (2008) Essential oils as green pesticides: potential and constraints. Biopesticides International 4, 6384.Google Scholar
Kubo, R and Ono, M (2010) Comparative analysis of volatile components from labial glands of male Japanese bumblebees (Bombus spp.). Entomological Science 13, 167173.CrossRefGoogle Scholar
Margaritopoulos, JT, Kasprowicz, L, Malloch, GL and Fenton, B (2009) Tracking the global dispersal of a cosmopolitan insect pest, the peach potato aphid. BMC Ecology 9, 113.CrossRefGoogle ScholarPubMed
Martin, B, Collar, L, Tjallingii, WF and Fereres, A (1997) Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. Journal of General Virology 78, 27012705.CrossRefGoogle ScholarPubMed
Martinez, S and Van Emden, H (1999) Sublethal concentrations of azadirachtin affect food intake, conversion efficiency and feeding behaviour of Spodoptera littoralis (Lepidoptera: Noctuidae). Bulletin of Entomological Research 89, 6571.CrossRefGoogle Scholar
Mayoral, AM, Tjallingii, WF and Castañera, P (1996) Probing behaviour of Diuraphis noxia on five cereal species with different hydroxamic acid levels. Entomologia Experimentalis et Applicata 78, 341348.CrossRefGoogle Scholar
Miles, P (1999) Aphid saliva. Biological Reviews 74, 4185.CrossRefGoogle Scholar
Moreno, A, Tjallingii, WF, Fernandez-Mata, G and Fereres, A (2012) Differences in the mechanism of inoculation between a semi-persistent and a non-persistent aphid-transmitted plant virus. Journal of General Virology 93, 662667.CrossRefGoogle Scholar
Mossa, ATH (2016) Green pesticides: essential oils as biopesticides in insect-pest management. Journal of Environmental Science and Technology 9, 354378.Google Scholar
Paprocka, M, Gliszczyńska, A, Dancewicz, K and Gabryś, B (2018) Novel hydroxy- and epoxy-cis-jasmone and dihydrojasmone derivatives affect the foraging activity of the peach potato aphid Myzus persicae (Sulzer) (Homoptera: Aphididae). Molecules, 23, 2362.CrossRefGoogle Scholar
Pettersson, J, Tjallingii, WF and Hardie, J (2017) Host-plant selection and feeding. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests. Wallingford, England: CABI. pp. 173195.CrossRefGoogle Scholar
Philippi, J, Schliephake, E, Jurgens, HU, Jansen, G and Ordon, F (2015) Feeding behavior of aphids on narrow-leafed lupin (Lupinus angustifolius) genotypes varying in the content of quinolizidine alkaloids. Entomologia Experimentalis et Applicata 156, 3751.CrossRefGoogle Scholar
Phuong, T, Wróblewska-Kurdyk, A, Dancewicz, K and Gabryś, B (2015) Selective acceptance of Brassicaceous plants by the peach potato aphid Myzus persicae: a case study of Aurinia saxatilis. Acta Biologica 846, 5162.Google Scholar
Pickett, JA, Wadhams, LJ and Woodcock, CM (1997) Developing sustainable pest control from chemical ecology. Agriculture, Ecosystems and Environment 64, 149156.CrossRefGoogle Scholar
Pickett, JA, Woodcock, CM, Midega, CAO and Khan, ZR (2014) Push–pull farming systems. Current Opinion in Biotechnology 26, 125132.CrossRefGoogle ScholarPubMed
Polonsky, J, Bhatnagar, SC, Griffiths, DC, Pickett, JA and Woodcock, CM (1989) Activity of quassinoids as antifeedants against aphids. Journal of Chemical Ecology 15, 993998.CrossRefGoogle ScholarPubMed
Powell, G, Maniar, SP, Pickett, JA and Hardie, J (1999) Aphid responses to non-host epicuticular lipids. Entomologia Experimentalis et Appicata 91, 115123.CrossRefGoogle Scholar
Ramírez, CC and Niemeyer, HM (1999) Salivation into sieve elements in relation to plant chemistry: the case of the aphid Sitobion fragariae and the wheat, Triticum aestivum. Entomologia Experimentalis et Applicata 91, 111114.CrossRefGoogle Scholar
Schliephake, E (2010) Aphid resistance in raspberry and feeding behaviour of Amphorophora idaei. Journal of Plant Diseases and Protection 117, 6066.CrossRefGoogle Scholar
Stompor, M, Dancewicz, K, Gabryś, B and Anioł, M (2015) Insect antifeedant potential of xanthohumol, isoxanthohumol, and their derivatives. Journal of Agricultural and Food Chemistry 63, 67496756.CrossRefGoogle ScholarPubMed
Strube-Bloss, MF, Brown, A, Spaethe, J, Schmitt, T and Rössler, W (2015) Extracting the behaviorally relevant stimulus: unique neural representation of farnesol, a component of the recruitment pheromone of Bombus terrestris. PLoS One 10, e0139296.CrossRefGoogle ScholarPubMed
Tjallingii, WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739745.CrossRefGoogle ScholarPubMed
Valenzuela, I and Hoffman, AA (2015) Effects of aphid feeding and associated virus injury on grain crops in Australia. Australian Entomologist 54, 292305.CrossRefGoogle Scholar
van Helden, M and Tjallingii, WF (1993) Tissue localisation of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Entomologia Experimentalis et Applicata 68, 269278.CrossRefGoogle Scholar
Vucetic, A, Dahlin, I, Petrovic-Obradovic, O, Glinwood, R, Webster, B and Ninkovic, V (2014) Volatile interaction between undamaged plants affects tritrophic interactions through changed plant volatile emission. Plant Signaling & Behavior 9, e29517.CrossRefGoogle ScholarPubMed
Wilkinson, TL and Douglas, AE (1998) Plant penetration by pea aphids (Acyrthosiphon pisum) of different plant range. Entomologia Experimentalis et Applicata 87, 4350.CrossRefGoogle Scholar
Wróblewska-Kurdyk, A, Nowak, L, Dancewicz, K, Szumny, A and Gabryś, B (2015) In search of biopesticides: the effect of caraway Carum carvi essential oil and its major constituents on peach potato aphid Myzus persicae probing behavior. Acta Biologica 22, 5162.Google Scholar