Biological activity and specificity of Miridae-induced plant volatiles

[EN] The ability of zoophytophagous predators to produce defensive plant responses due to their phytophagous behavior has been recently demonstrated. In the case of tomatoes, the mirids Nesidiocoris tenuis and Macrolophus pygmaeus are able to attract or repel pests and/or natural enemies in different ways. Nevertheless, the herbivore-induced plant volatiles (HIPVs) released by the phytophagy of both mirids, which are responsible for these behaviors, are unknown. In this work, the HIPVs produced by the plant feeding of N. tenuis and M. pygmaeus were characterized. In addition, the role of each HIPV in the repellence or attraction of two tomato pests, Bemisia tabaci and Tuta absoluta, and of the natural enemy Encarsia formosa was evaluated. Six green leaf volatiles (GLVs) plus methyl salicylate and octyl acetate clearly stood out as major differential peaks on the chromatogram in a directed analysis. The six GLV and methyl salicylate were repellent for B. tabaci and attractive to E. formosa, whereas they showed no effect on T. absoluta. Octyl acetate, which was significantly present only in the M. pygmaeus-punctured plants, was significantly attractive to T. absoluta, repellent to E. formosa and indifferent to B. tabaci. Unlike the remaining HIPVs, octyl acetate was emitted directly by M. pygmaeus and not by the plant. Our results showed that mirid herbivory could modulate the pest and natural plant enemy locations, since tomato plants release a blend of volatiles in response to this activity. These results could serve as a basis for future development of plant protection.The research leading to these results was funded by the Spanish Ministry of Economy and Competitiveness (AGL2014-55616-C3). The authors thank Javier Calvo (KOPPERT BS) for the supply of insects, and Sandra Fresquet and Virginia Pedroche for their technical assistance. MP-H was the recipient of a research fellowship from the INIA Spain (Subprogram DOC-INIA-CCAA). Analyses of volatile compounds were performed in the Metabolomics service facilities at IBMCP.Pérez-Hedo, M.; Granell Richart, A.; Rambla Nebot, JL.; Urbaneja Garcia, A. (2017). Biological activity and specificity of Miridae-induced plant volatiles. BioControl. 63(2):203-213. https://doi.org/10.1007/s10526-017-9854-4203213632Abbas S, Pérez-Hedo M, Colazza S, Urbaneja A (2014) The predatory mirid Dicyphus maroccanus as a new potential biological control agent in tomato crops. BioControl 59:565–574Ardanuy A, Albajes R, Turlings TC (2016) Innate and learned prey-searching behavior in a generalist predator. J Chem Ecol 42:497–507Arnó J, Gabarra R, Liu TX, Simmons AM, Gerling D (2010) Natural enemies of Bemisia tabaci: predators and parasitoids. In: Stansly PA, Naranjo SE (eds) Bemisia: bionomics and management of a global pest. Springer, Dordrecht, pp 385–421Attygalle AB, Jham GN, Svatos A, Frighetto RTS, Ferrara FA, Vilela EF, Uchôa-Fernandes MA, Meinwald J (1996) 3E,8Z,11Z)-3,8,11-tetradecatrienyl acetate, major sex pheromone component of the tomato pest Scrobipalpuloides absoluta (Lepidoptera: Gelechiidae. Bioorg Med Chem 4:305–314Barnadas I, Gabarra R, Albajes R (1998) Predatory capacity of two mirid bugs preying on Bemisia tabaci. Entomol Exp Appl 86:215–219Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol Exp Appl 87:133–142Biondi A, Zappalà L, Di Mauro A, Tropea Garzia G, Russo A, Desneux N, Siscaro G (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? BioControl 61:79–90Bukovinszky T, Gols R, Posthumus MA, Vet LE, van Lenteren JC (2005) Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellén). J Chem Ecol 31:461–480Calvo FJ, Bolckmans K, Stansly PA, Urbaneja A (2009) Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato. BioControl 54:237–246Calvo FJ, Soriano J, Bolckmans K, Belda JE (2012) A successful method for whitefly and Tuta absoluta control in tomato. Evaluation after two years of application in practice. IOBC/WPRS Bull 80:237–244Castañé C, Arnó J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol Exp Appl 91:131–142Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902Eubanks MD, Denno RF (1999) The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80:1253–1266Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824Gillespie DR, Mcgregor RR (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation. Ecol Entomol 25:380–386Giunti G, Benelli G, Palmeri V, Canale A (2017) Bactrocera oleae-induced olive VOCs routing mate searching in Psyttalia concolor males: impact of associative learning. Bull Entomol Res. https://doi.org/10.1017/S0007485317000451James DG (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495Kappers IF, Aharoni A, van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144Leitner M, Boland W, Mithöfer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167:597–606Levi-Zada A, Sadowsky A, Dobrinin S, David M, Ticuchinski T, Fefer D, Greenberg A, Blumberg D (2013) Reevaluation of the sex pheromone of the lesser date moth, Batrachedra amydraula, using autosampling SPME-GC/MS and field bioassays. Chemoecology 23:13–24Messelink GJ, Bloemhard CMJ, Hoogerbrugge H, van Schelt J, Ingegno BL, Tavella L (2015) Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper. J Appl Entomol 139:333–341Millar JG, Rice RE (1998) Sex pheromone of the plant bug Phytocoris californicus (Heteroptera: Miridae). J Econ Entomol 91:132–137Millar JG, Rice RE, Wang Q (1997) Sex pheromone of the mirid bug Phytocoris relativus. J Chem Ecol 23:1743–1754Naselli M, Urbaneja A, Siscaro G, Jaques JA, Zappalà L, Flors V, Pérez-Hedo M (2016a) Stage-related defense response induction in tomato plants by Nesidiocoris tenuis. Int J Mol Sci 17:1210–1223Naselli M, Zappalà L, Gugliuzzo A, Tropea Garzia G, Biondi A, Rapisarda C, Cincotta F, Condurso C, Verzera A, Siscaro G (2016b) Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod-Plant Interact 11:121–131Ozawa R, Shiojiri K, Sabelis MW, Takabayashi J (2008) Maize plants sprayed with either jasmonic acid or its precursor, methyl linolenate, attract armyworm parasitoids, but the composition of attractants differs. Entomol Exp Appl 129:189–199Pappas ML, Steppuhn A, Geuss D, Topalidou N, Zografou A, Sabelis MW, Broufas GD (2015) Beyond predation: the zoophytophagous predator Macrolophus pygmaeus induces tomato resistance against spider mites. PLoS ONE 10(5):e0127251Paré PW, Tumlinson JH (1999) Plant volatiles as a defence against insect herbivores. Plant Physiol 121:325–331Perdikis D, Fantinou A, Lykouressis D (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control 59:13–21Pérez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73Pérez-Hedo M, Urbaneja A (2016) The zoophytophagous predator Nesidiocoris tenuis: a successful but controversial biocontrol agent in tomato crops. In: Horowitz AR, Ishaaya I (eds) Advances in insect control and resistance management. Springer International Publishing, Cham, pp 121–138Pérez-Hedo M, Suay R, Alonso M, Ruocco M, Giorgini M, Poncet C, Urbaneja A (2017) Resilience and robustness of IPM in protected horticulture in the face of potential invasive pests. Crop Prot 97:119–127Pérez-Hedo M, Urbaneja-Bernat P, Jaques JA, Flors V, Urbaneja A (2015a) Defensive plant responses induced by Nesidiocoris tenuis (Hemiptera: Miridae) on tomato plants. J Pest Sci 88:543–554Pérez-Hedo M, Bouagga S, Jaques JA, Flors V, Urbaneja A (2015b) Tomato plant responses to feeding behavior of three zoophytophagous predators (Hemiptera: Miridae). Biol Control 86:46–51Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303Sabelis MW, Janssen A, Pallini A, Venzon M, Bruin J, Drukker B, Scutareanuu P (1999) Behavioural responses of predatory and herbivorous arthropods to induced plant volatiles: From evolutionary ecology to agricultural applications. In: Agrawal A, Tuzun S, Bent E (eds) Induced plant defenses against pathogens and herbivores. American Phytopathological Society Press, St. Paul, pp 269–296Sanchez JA (2009) Density thresholds for Nesidiocoris tenuis (Heteroptera: Miridae) in tomato crops. Biol Control 51:493–498Sanchez JA, Gillespie DR, McGregor RR (2004) Plant preference in relation to life history traits in the zoophytophagous predator Dicyphus hesperus. Entomol Exp Appl 112:7–19Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, Arimura G, Horiuchi J, Nishioka T, Matsui K, Takabayashi J (2006) Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc Natl Acad Sci USA 103:16672–16676Sinia A, Roitberg B, McGregor RR, Gillespie DR (2004) Prey feeding increases water stress in the omnivorous predator Dicyphus hesperus. Entomol Exp Appl 110:243–248Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz G, Dorn S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129Ulland S, Ian E, Mozuraitis R, Borg-Karlson AK, Meadow R, Mustaparta H (2008) Methyl salicylate, identified as primary odorant of a specific receptor neuron type, inhibits oviposition by the moth Mamestra brassicae L. (Lepidoptera, Noctuidae). Chem Senses 33:35–46Urbaneja A, Tapia G, Stansly P (2005) Influence of host plant and prey availability on developmental time and survivorship of Nesidiocoris tenuis (Het.: Miridae). Biocontrol Sci Techn 15:513–518Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus caliginosus and Nesidiocoris tenuis. J Appl Entomol 133:292–296Urbaneja A, González-Cabrera J, Arnó J, Gabarra R (2012) Prospects for the biological control of Tuta absoluta in tomatoes of the Mediterranean basin. Pest Manag Sci 68:1215–1222van Lenteren J, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2017) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl. https://doi.org/10.1007/s10526-017-9801-4Wager BR, Breed MD (2000) Does honey bee sting alarm pheromone give orientation information to defensive bees? Ann Entomol Soc Am 93:1329–1332Wang Z, Wen P, Qu Y, Dong S, Li J, Tan K, Nieh JC (2016) Bees eavesdrop upon informative and persistent signal compounds in alarm pheromones. Sci Rep-UK 6:25693War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320Yamashita KI, Isayama S, Ozawa R, Uefune M, Takabayashi J, Miura K (2016) A pecky rice-causing stink bug Leptocorisa chinensis escapes from volatiles emitted by excited conspecifics. J Ethol 34:1–7Zappala L, Biondi A, Alma A, Al-Jboory IJ, Arno J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Aznar RV, Urbaneja A, Desneux N (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86:635–647Zappalà L, Siscaro G, Biondi A, Mollá O, González-Cabrera J, Urbaneja A (2012) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J App Entomol 136:401–409Zhang QH, Aldrich JR (2008) Sex pheromone of the plant bug, Phytocoris calli Knight. J Chem Ecol 34:719–724Zhou S, Lou YR, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–149