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- W1856292377 abstract "Hundreds of studies convincingly demonstrate functioning indirect defenses in wild plants, but breeding approaches have never considered the underlying traits (e.g., food rewards or shelter for carnivores, and volatiles that mediate information-based interactions) as desirable targets. We argue that induced plant volatiles, owing to their multiple roles as signals, repellents, and antimicrobial compounds, bear an as-yet underused potential for biological control, and that future breeding efforts should enhance the capacity of crops to engage in tritrophic interactions. We also present ecological and evolutionary considerations that can explain why the constitutive release of volatile compounds that have evolved as inducible defenses is not likely to work, and why extrafloral nectar is likely to represent a better food reward for carnivores than floral nectar. Volatile compounds and extrafloral nectar are common defenses of wild plants; however, in crops they bear an as-yet underused potential for biological control of pests and diseases. Odor emission and nectar secretion are multigene traits in wild plants, and thus form difficult targets for breeding. Furthermore, domestication has changed the capacity of crops to express these traits. We propose that breeding crops for an enhanced capacity for tritrophic interactions and volatile-mediated direct resistance to herbivores and pathogens can contribute to environmentally-friendly and sustainable agriculture. Natural plant volatiles with antifungal or repellent properties can serve as direct resistance agents. In addition, volatiles mediating tritrophic interactions can be combined with nectar-based food rewards for carnivores to boost indirect plant defense. Volatile compounds and extrafloral nectar are common defenses of wild plants; however, in crops they bear an as-yet underused potential for biological control of pests and diseases. Odor emission and nectar secretion are multigene traits in wild plants, and thus form difficult targets for breeding. Furthermore, domestication has changed the capacity of crops to express these traits. We propose that breeding crops for an enhanced capacity for tritrophic interactions and volatile-mediated direct resistance to herbivores and pathogens can contribute to environmentally-friendly and sustainable agriculture. Natural plant volatiles with antifungal or repellent properties can serve as direct resistance agents. In addition, volatiles mediating tritrophic interactions can be combined with nectar-based food rewards for carnivores to boost indirect plant defense. Crop domestication aims to enhance the quality of plants for human use. In addition to yield, domestication (see Glossary) most commonly has altered the size, taste, and nutritional quality of the plant parts of interest, favoring synchronous ripening, homogenous plant sizes, apical dominance, determinate growth, indehiscent fruits, or other characteristics of relevance for cultivation and harvesting, as well as modifying traits that facilitate transport and storage [1Evans L.T. Crop Evolution, Adaptation and Yield. Cambridge University Press, 1996Google Scholar, 2Hammer K. Das Domestikationssyndrom.Kulturpflanze. 1984; 32: 11-34Crossref Scopus (0) Google Scholar, 3Andersen M.M. et al.Feasibility of new breeding techniques for organic farming.Trends Plant Sci. 2015; 20: 426-434Abstract Full Text Full Text PDF PubMed Google Scholar]. Furthermore, enhanced resistance to pathogens or abiotic stress represents an integrated goal in most plant breeding programs [4Dangl J.L. et al.Pivoting the plant immune system from dissection to deployment.Science. 2013; 341: 746-751Crossref PubMed Scopus (296) Google Scholar, 5Hammond-Kosack K.E. Parker J.E. Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding.Curr. Opin. Biotechnol. 2003; 14: 177-193Crossref PubMed Scopus (0) Google Scholar]. Breeding for resistance to herbivores (‘pests’) is less common [3Andersen M.M. et al.Feasibility of new breeding techniques for organic farming.Trends Plant Sci. 2015; 20: 426-434Abstract Full Text Full Text PDF PubMed Google Scholar, 6Godfray H.C.J. et al.Food security: the challenge of feeding 9 billion people.Science. 2010; 327: 812-818Crossref PubMed Scopus (2625) Google Scholar, 7Tamiru A. et al.New directions for improving crop resistance to insects by breeding for egg induced defence.Curr. Opin. Insect Sci. 2015; (Published online February 28, 2015)https://doi.org/10.1016/j.cois.2015.02.011Crossref Scopus (15) Google Scholar], although wild plants express multiple traits to resist herbivory. Therefore, ‘rewilding’ has become a new trend in crop breeding that opens exciting opportunities for biological control and organic farming. However, multiple regulatory and political issues currently impede the use of most genetic techniques to provide cultivars with specific resistance traits, particularly when these cultivars are to be used in organic farming [3Andersen M.M. et al.Feasibility of new breeding techniques for organic farming.Trends Plant Sci. 2015; 20: 426-434Abstract Full Text Full Text PDF PubMed Google Scholar]. Many resistance-related traits are inducible [8Arimura G. et al.Herbivore-induced, indirect plant defences.Biochim. Biophys. Acta Mol. Cell Biol. Lipids. 2005; 1734: 91-111Crossref PubMed Scopus (0) Google Scholar, 9Walling L.L. The myriad plant responses to herbivores.J. Plant Growth Regul. 2000; 19: 195-216PubMed Google Scholar] or can be primed for a faster and stronger induction once damage occurs [10Conrath U. et al.Priming: getting ready for battle.Mol. Plant Microbe Interact. 2006; 19: 1062-1071Crossref PubMed Scopus (648) Google Scholar, 11Frost C. et al.Plant defense priming against herbivores: getting ready for a different battle.Plant Physiol. 2008; 146: 818-824Crossref PubMed Scopus (193) Google Scholar]. This phenotypic plasticity helps to balance costs and benefits of defense expression because it assures that costly defenses are only expressed when they are actually required [12Karban R. Baldwin I.T. Induced Responses to Herbivory. University of Chicago Press, 1997Crossref Google Scholar, 13Heil M. Plastic defence expression in plants.Evol. Ecol. 2010; 24: 555-569Crossref Scopus (0) Google Scholar]. Among the inducible traits, seemingly all plants respond to herbivore-inflicted damage with the enhanced emission of volatile organic compounds (VOCs), and plants in numerous taxa also respond with the secretion of extrafloral nectar (EFN) [14Karban R. The ecology and evolution of induced resistance against herbivores.Funct. Ecol. 2011; 25: 339-347Crossref Scopus (165) Google Scholar, 15Heil M. Herbivore-induced plant volatiles: targets, perception and unanswered questions.New Phytol. 2014; 204: 297-306Crossref Scopus (58) Google Scholar, 16Unsicker S.B. et al.Protective perfumes: the role of vegetative volatiles in plant defense against herbivores.Curr. Opin. Plant Biol. 2009; 12: 479-485Crossref PubMed Scopus (178) Google Scholar, 17Dudareva N. et al.Plant volatiles: recent advances and future perspectives.Crit. Rev. Plant Sci. 2006; 25: 417-440Crossref Scopus (471) Google Scholar]. Both VOCs and EFN attract adult parasitoids and predators (hereinafter collectively termed ‘carnivores’), an effect that can significantly reduce herbivore pressure on wild plants [18Heil M. Indirect defence via tritrophic interactions.New Phytol. 2008; 178: 41-61Crossref PubMed Scopus (382) Google Scholar, 19Heil M. Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs.Annu. Rev. Entomol. 2015; 60: 213-232Crossref PubMed Google Scholar]. Nevertheless, relatively few attempts have made conscious use of VOCs or EFN for biological pest control [20Khan Z.R. et al.Achieving food security for one million sub-Saharan African poor through push-pull innovation by 2020.Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2014; (0120284): 369Google Scholar, 21Atanassov A. Shearer P. Peach extrafloral nectar impacts life span and reproduction of adult Grapholita molesta (Busck) (Lepidoptera: Tortricidae).J. Agric. Urban Entomol. 2005; 22: 41-47Google Scholar, 22Brown M.W. et al.Extrafloral nectar in an apple ecosystem to enhance biological control.J. Econ. Entomol. 2010; 103: 1657-1664Crossref PubMed Scopus (0) Google Scholar, 23Mathews C.R. et al.Interactions between extrafloral nectaries, ants (Hymenoptera: Formicidae), and other natural enemies affect biological control of Grapholita molesta (Lepidoptera: Tortricidae) on Peach (Rosales: Rosaceae).Environ. Entomol. 2011; 40: 42-51Crossref PubMed Scopus (0) Google Scholar, 24James D.G. Price T.S. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops.J. Chem. Ecol. 2004; 30: 1613-1628Crossref PubMed Scopus (0) Google Scholar, 25Orre-Gordon G.U.S. et al.‘Attract and reward’: combining a herbivore-induced plant volatile with floral resource supplementation – multi-trophic level effects.Biol. Contr. 2013; 64: 106-115Crossref Scopus (0) Google Scholar, 26Mérey G.v. et al.Dispensing synthetic green leaf volatiles in maize fields increases the release of sesquiterpenes by the plants, but has little effect on the attraction of pest and beneficial insects.Phytochemistry. 2011; 72: 1838-1847Crossref PubMed Scopus (0) Google Scholar] and, to the best of our knowledge, classical breeding has never aimed to improve anti-herbivore defense via VOCs or EFN [1Evans L.T. Crop Evolution, Adaptation and Yield. Cambridge University Press, 1996Google Scholar, 27Åhman I. et al.The potential for modifying plant volatile composition to enhance resistance to arthropod pests.CAB Rev. Perspect. Agricul. Vet. Sci., Nutr. Nat. Res. 2010; 5: 006Google Scholar] (but see [28Bruce T.J.A. et al.The first crop plant genetically engineered to release an insect pheromone for defence.Sci. Rep. 2015; 5: 11183Crossref PubMed Google Scholar] for the first attempt to genetically engineer wheat (Triticum aestivum) for the emission of an aphid alarm pheromone as a means to enhance repellence of aphids and attract aphid carnivores). We highlight the major defensive functions of VOCs and EFN, discuss why VOCs and EFN are rarely included in breeding programs, and propose how and to what degree these traits can be optimized to allow better biological control of pests and crop diseases. Plants express multiple traits that provide resistance to the majority of potential herbivores and pathogens [29Barrett L.G. Heil M. Unifying concepts and mechanisms in the specificity of plant–enemy interactions.Trends Plant Sci. 2012; 17: 282-292Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. Many traits act directly against these enemies via their toxic, repellent, or antimicrobial effects or function as mechanical barriers, but other resistance strategies work indirectly [18Heil M. Indirect defence via tritrophic interactions.New Phytol. 2008; 178: 41-61Crossref PubMed Scopus (382) Google Scholar]. For example, plants release an array of VOCs when damaged [30Dicke M. Sabelis M.W. How plants obtain predatory mites as bodyguards.Netherlands J. Zool. 1988; 38: 148-165Crossref Scopus (0) Google Scholar, 31Turlings T.C.J. et al.Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.Science. 1990; 250: 1251-1253Crossref PubMed Google Scholar, 32Dicke M. Baldwin I.T. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’.Trends Plant Sci. 2010; 15: 167-175Abstract Full Text Full Text PDF PubMed Scopus (460) Google Scholar], and the particular blends depend on the type of wound and even the type of attacker [33Clavijo McCormick A. et al.The specificity of herbivore-induced plant volatiles in attracting herbivore enemies.Trends Plant Sci. 2012; 17: 303-310Abstract Full Text Full Text PDF PubMed Scopus (140) Google Scholar, 34Dicke M. et al.Chemical complexity of volatiles from plants induced by multiple attack.Nat. Chem. Biol. 2009; 5: 317-324Crossref PubMed Scopus (208) Google Scholar]. Because such induced VOCs frequently indicate the presence of a herbivore, they are utilized by many carnivores as cues to find their prey, a behavior that can reduce herbivore loads and thus cause ‘indirect’ defense of the plants [35Kessler A. Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature.Science. 2001; 291: 2141-2144Crossref PubMed Scopus (1140) Google Scholar]. Studies searching for beneficial effects of VOCs have reported multiple promising observations (Table 1), including enhanced recruitment of predators, parasitoids, or entomopathogenic nematodes to VOC-releasing plants [30Dicke M. Sabelis M.W. How plants obtain predatory mites as bodyguards.Netherlands J. Zool. 1988; 38: 148-165Crossref Scopus (0) Google Scholar, 31Turlings T.C.J. et al.Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.Science. 1990; 250: 1251-1253Crossref PubMed Google Scholar, 35Kessler A. Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature.Science. 2001; 291: 2141-2144Crossref PubMed Scopus (1140) Google Scholar, 36Rasmann S. et al.Recruitment of entomopathogenic nematodes by insect-damaged maize roots.Nature. 2005; 434: 732-737Crossref PubMed Scopus (618) Google Scholar, 37de Moraes C.M. et al.Herbivore-infested plants selectively attract parasitoids.Nature. 1998; 393: 570-573Crossref Scopus (0) Google Scholar], enhanced parasitization rates in caterpillars that were reared close to VOC-emitting plants [38Thaler J.S. Jasmonate-inducible plant defences cause increased parasitism of herbivores.Nature. 1999; 399: 686-688Crossref Scopus (0) Google Scholar], the successful use of intercropping with plant neighbors that mimic the emission of herbivore-induced VOCs [39Khan Z.R. et al.Intercropping increases parasitism of pests.Nature. 1997; 388: 631-632Crossref Google Scholar] or with repellent crops to ‘push’ pests out of maize fields and ‘pull’ them into surrounding trap plants [20Khan Z.R. et al.Achieving food security for one million sub-Saharan African poor through push-pull innovation by 2020.Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2014; (0120284): 369Google Scholar, 40Hassanali A. et al.Integrated pest management: the push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry.Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008; 363: 611-621Crossref PubMed Scopus (0) Google Scholar] (Figure 1), and enhanced density of parasitoids close to dispensers emitting, for example, the VOC methyl salicylate (MeSA) [24James D.G. Price T.S. Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops.J. Chem. Ecol. 2004; 30: 1613-1628Crossref PubMed Scopus (0) Google Scholar, 41Braasch J. Kaplan I. Over what distance are plant volatiles bioactive? Estimating the spatial dimensions of attraction in an arthropod assemblage.Entomol. Exp. Appl. 2012; 145: 115-123Crossref Scopus (0) Google Scholar, 42Kaplan I. Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire?.Biol. Contr. 2012; 60: 77-89Crossref Scopus (0) Google Scholar, 43Turlings T.C.J. Ton J. Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests.Curr. Opin. Plant Biol. 2006; 9: 421-427Crossref PubMed Scopus (0) Google Scholar, 44Kelly J.L. et al.Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation.Biol. Contr. 2014; 71: 70-77Crossref Scopus (0) Google Scholar].Table 1Examples of Direct and Indirect Resistance Effects for Application in BiocontrolPlant SpeciesEnvironmentTreatmentResponse ObservedRefsBarley (Hordeum vulgare)LaboratoryPlants infested by aphid (Rhopalosiphum padi)Attraction of the predatory beetle, Coccinella septempunctata121Ninkovic V. et al.The influence of aphid-induced plant volatiles on ladybird beetle searching behavior.Biol. Contr. 2001; 21: 191-195Crossref Scopus (0) Google ScholarBirch (Betula pubescens)FieldPresence of herbivore-damaged leaves or methyl jasmonate (MeJA) treatmentAttraction of insectivorous birds122Mäntylä E. et al.From plants to birds: higher avian predation rates in trees responding to insect herbivory.PLoS ONE. 2008; 3: e2832Crossref PubMed Scopus (0) Google Scholar, 123Mäntylä E. et al.Does application of methyl jasmonate to birch mimic herbivory and attract insectivorous birds in nature?.Athrop. Plant Interact. 2014; 8: 143-153Crossref Scopus (0) Google ScholarBean (Phaseolus vulgaris)FieldExposure to inoculated or Benzothiadiazole (BTH)-treated emitter plantEnhanced resistance to the fungal pathogen, Colletotrichum lindemuthianum, priming of PR-1, 2, and 4, and direct inhibition of fungal spore germination on the leaf surface62Quintana-Rodriguez E. et al.Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum.J. Ecol. 2015; 103: 250-260Crossref Scopus (0) Google ScholarCotton (Gossypium hirsutum)Field and CageHerbivore-damaged plantsRepellence of adult females of the herbivore, Spodoptera littoralis124Zakir A. et al.Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore.J. Ecol. 2013; 101: 410-417Crossref Scopus (0) Google ScholarMaize (Zea mays)LaboratoryApplication of caterpillar oral secretion to wounded leaf tissueFemales of parasitic wasp Cotesia marginiventris learn to respond to the released VOCs31Turlings T.C.J. et al.Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps.Science. 1990; 250: 1251-1253Crossref PubMed Google ScholarMaize (Zea mays)FieldDamage by root-feeding Diabrotica larvaeAttraction of entomopathogenic nematodes36Rasmann S. et al.Recruitment of entomopathogenic nematodes by insect-damaged maize roots.Nature. 2005; 434: 732-737Crossref PubMed Scopus (618) Google ScholarMaize (Zea mays)FieldIntercropping with the grass, Melinis minutifloraIncreased levels of infestation by stem-borers and enhanced parasitization rates of these39Khan Z.R. et al.Intercropping increases parasitism of pests.Nature. 1997; 388: 631-632Crossref Google ScholarLima bean (Phaseolus lunatus)LaboratoryDamage inflicted by the spider mite, Tetranychus urticaeEnhanced attraction of the predatory mite, Phytoseiulus persimilis30Dicke M. Sabelis M.W. How plants obtain predatory mites as bodyguards.Netherlands J. Zool. 1988; 38: 148-165Crossref Scopus (0) Google ScholarLima bean (Phaseolus lunatus)FieldSupplementation of EFNEnhanced number of ants, decreased rates of herbivory, and enhanced seed set125Kost C. Heil M. The defensive role of volatile emission and extrafloral nectar secretion for Lima bean in nature.J. Chem. Ecol. 2008; 34: 2-13Crossref Scopus (0) Google ScholarLima bean (Phaseolus lunatus)LaboratoryTreatment with jasmonic acid (JA)Adult females of the herbivorous beetles, Gynandrobrotica guerreroensi and Cerotoma ruficornis, preferred controls over induced plants77Ballhorn D.J. et al.Distance and sex determine host plant choice by herbivorous beetles.PLoS ONE. 2013; 8: e55602Crossref PubMed Scopus (0) Google ScholarLima bean (Phaseolus lunatus)LaboratoryExposure to conspecific plants treated with BTH or to the pure VOC, nonanalEnhanced resistance to pathogenic bacterium, Pseudomonas syringae, and priming of PR-270Yi H-S. et al.Airborne induction and priming of plant resistance to a bacterial pathogen.Plant Physiol. 2009; 151: 2152-2161Crossref PubMed Scopus (0) Google ScholarWild tobacco (Nicotiana attenuata)Release of cis-3-hexen-1-ol, linalool, and cis-α -bergamoteneIncreased herbivore egg predation rates by a generalist predator (Geocoris pallens)35Kessler A. Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature.Science. 2001; 291: 2141-2144Crossref PubMed Scopus (1140) Google ScholarWild tobacco (Nicotiana attenuata)Linalool and the complete blend of MeJA-treated plantDecreased lepidopteran (Manduca quinquemaculata) oviposition rates35Kessler A. Baldwin I.T. Defensive function of herbivore-induced plant volatile emissions in nature.Science. 2001; 291: 2141-2144Crossref PubMed Scopus (1140) Google ScholarTomato (Lycopersicon esculentum)FieldExogenous application of JAHigher parasitization rates of caged caterpillars38Thaler J.S. Jasmonate-inducible plant defences cause increased parasitism of herbivores.Nature. 1999; 399: 686-688Crossref Scopus (0) Google ScholarTobacco (Nicotiana tabacum)FieldDamage by different herbivoresFemales of the specialist parasitoid (Cardiochiles nigriceps) distinguish plants damaged by hosts vs non-host caterpillars37de Moraes C.M. et al.Herbivore-infested plants selectively attract parasitoids.Nature. 1998; 393: 570-573Crossref Scopus (0) Google ScholarTobacco plants (Nicotiana tabacum)GreenhouseDamage by Heliothis virescence caterpillarsRepellence of conspecific females126de Moraes C.M. et al.Caterpillar-induced nocturnal plant volatiles repel conspecific females.Nature. 2001; 410: 577-580Crossref PubMed Scopus (0) Google Scholar Open table in a new tab In addition to VOCs, plants commonly attract and maintain carnivores by offering shelter (such as domatia in the form of cavities or trichome tufts for ants and mites) or food rewards [such as pollen, floral nectar (FN), extrafloral nectar (EFN), and plant sap] [18Heil M. Indirect defence via tritrophic interactions.New Phytol. 2008; 178: 41-61Crossref PubMed Scopus (382) Google Scholar]. These rewards contain carbohydrates and amino acids, and are consumed by a diverse range of carnivores [18Heil M. Indirect defence via tritrophic interactions.New Phytol. 2008; 178: 41-61Crossref PubMed Scopus (382) Google Scholar], most frequently during the adult stage [19Heil M. Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs.Annu. Rev. Entomol. 2015; 60: 213-232Crossref PubMed Google Scholar, 45Lundgren J.G. Relationships of Natural Enemies and Non-Prey Foods. Springer, 2009Google Scholar, 46Narvaez A. et al.Effect of different dietary resources on longevity, carbohydrate metabolism, and ovarian dynamics in two fruit fly parasitoids.Arthropod Plant Interact. 2012; 6: 361-374Crossref Scopus (0) Google Scholar, 47Wäckers F.L. et al.Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge University Press, 2005Crossref Google Scholar]. In particular, the ingestion of nectar enhances the longevity and predatory efficiency of carnivores or reduces intraguild predation [48Stenberg J.A. et al.Uncoupling direct and indirect plant defences: novel opportunities for improving crop security in willow plantations.Agricul. Ecosyst. Environ. 2010; 139: 528-533Crossref Scopus (0) Google Scholar, 49Stenberg J.A. et al.Host-plant genotype mediates supply and demand of animal food in an omnivorous insect.Ecol. Entomol. 2011; 36: 442-449Crossref Scopus (11) Google Scholar, 50Ferreira J.A.M. et al.Leaf domatia reduce intraguild predation among predatory mites.Ecol. Entomol. 2011; 36: 435-441Crossref Scopus (0) Google Scholar]. These food rewards affect the performance, behavior, and voracity of carnivores [19Heil M. Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs.Annu. Rev. Entomol. 2015; 60: 213-232Crossref PubMed Google Scholar, 45Lundgren J.G. Relationships of Natural Enemies and Non-Prey Foods. Springer, 2009Google Scholar, 47Wäckers F.L. et al.Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge University Press, 2005Crossref Google Scholar, 48Stenberg J.A. et al.Uncoupling direct and indirect plant defences: novel opportunities for improving crop security in willow plantations.Agricul. Ecosyst. Environ. 2010; 139: 528-533Crossref Scopus (0) Google Scholar, 49Stenberg J.A. et al.Host-plant genotype mediates supply and demand of animal food in an omnivorous insect.Ecol. Entomol. 2011; 36: 442-449Crossref Scopus (11) Google Scholar], an effect that can be used to optimize the efficacy of biological control by using plant genotypes of a desired quality [51Ågren G.I. et al.Omnivores as plant bodyguards – a model of the importance of plant quality.Basic Appl. Ecol. 2012; 13: 441-448Crossref Scopus (9) Google Scholar]. In particular, the secretion of EFN usually reduces herbivory on the respective plants [52Chamberlain S.A. Holland J.N. Quantitative synthesis of context dependency in ant-plant protection mutualisms.Ecology. 2009; 90: 2384-2392Crossref PubMed Scopus (0) Google Scholar, 53Romero G.Q. Koricheva J. Contrasting cascade effects of carnivores on plant fitness: a meta-analysis.J. Anim. Ecol. 2011; 80: 696-704Crossref PubMed Scopus (39) Google Scholar, 54Rosumek F.B. et al.Ants on plants: a meta-analysis of the role of ants as plant biotic defenses.Oecologia. 2009; 160: 537-549Crossref PubMed Scopus (166) Google Scholar]. In the horticultural context, there are reports of enhanced protection from herbivores in plants that secrete EFN [22Brown M.W. et al.Extrafloral nectar in an apple ecosystem to enhance biological control.J. Econ. Entomol. 2010; 103: 1657-1664Crossref PubMed Scopus (0) Google Scholar, 55Mathews C.R. et al.Extrafloral nectaries alter arthropod community structure and mediate peach (Prunus persica) plant defense.Ecol. Appl. 2009; 19: 722-730Crossref PubMed Scopus (0) Google Scholar, 56Mathews C.R. et al.Leaf extrafloral nectaries enhance biological control of a key economic pest, Grapholita molesta (Lepidoptera: Tortricidae), in peach (Rosales: Rosaceae).Environ. Entomol. 2007; 36: 383-389Crossref PubMed Google Scholar], produce large amounts of pollen [57Abdala-Roberts L. et al.Plant traits mediate effects of predators across pepper (Capsicum annuum) varieties.Ecol. Entomol. 2014; 39: 361-370Crossref Google Scholar], or provide additional shelter to ants or predatory mites [58Agrawal A.A. Karban R. Domatia mediate plant-arthropod mutualism.Nature. 1997; 387: 562-563Crossref Scopus (0) Google Scholar]. The availability of carbohydrates is a common bottleneck for carnivores, whereas herbivores are usually limited by the supply of proteins. Therefore, carbohydrate-based rewards can shift the balance in favor of the third trophic level [19Heil M. Extrafloral nectar at the plant–insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs.Annu. Rev. Entomol. 2015; 60: 213-232Crossref PubMed Google Scholar], even when a specific reward happens to be used by herbivores as well. Similarly, domatia are usually occupied by predators rather than herbivores [18Heil M. Indirect defence via tritrophic interactions.New Phytol. 2008; 178: 41-61Crossref PubMed Scopus (382) Google Scholar, 58Agrawal A.A. Karban R. Domatia mediate plant-arthropod mutualism.Nature. 1997; 387: 562-563Crossref Scopus (0) Google Scholar, 59Agrawal A.A. et al.How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance.Oikos. 2000; 89: 70-80Crossref Google Scholar], and thus should favor predators more than herbivores. Finally, several green leaf volatiles (GLVs) [60Scala A. et al.Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens.Int. J. Mol. Sci. 2013; 14: 17781-17811Crossref PubMed Scopus (0) Google Scholar, 61Turlings T.C.J. et al.Timing of induced volatile emissions in maize seedlings.Planta. 1998; 207: 146-152Crossref Scopus (0) Google Scholar] and other VOCs, that are quickly released in response to injury, have direct antimicrobial effects and thereby contribute to an immediate resistance to disease, both in the damaged plant and in its neighbors [15Heil M. Herbivore-induced plant volatiles: targets, perception and unanswered questions.New Phytol. 2014; 204: 297-306Crossref Scopus (58) Google Scholar, 60Scala A. et al.Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens.Int. J. Mol. Sci. 2013; 14: 17781-17811Crossref PubMed Scopus (0) Google Scholar, 62Quintana-Rodriguez E. et al.Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum.J. Ecol. 2015; 103: 250-260Crossref Scopus (0) Google Scholar]. For example, MeSA represents the volatile form of salicylic acid (SA), a central regulator of induced plant resistance to biotrophic pathogens [63Park S.W. et al.Methyl salicylate is a critical mobile signal for plant systemic acquired resistance.Science. 2007; 318: 113-116Crossref PubMed Scopus (0) Google Scholar]. (Z)-3-hexenal and its isomer, (E)-2-hexenal, inhibit the growth of several strains of bacteria and the pathogenic fungus Botrytis cinerea (see [60Scala A. et al.Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens.Int. J. Mol. Sci. 2013; 14: 17781-17811Crossref PubMed Scopus (0) Google Scholar] for review), and monoterpenes such as linalool and limonene at natural concentrations can inhibit the germination of conidia of the pathogenic fungus, Colletotrichum lindemuthianum, on bean plants [62Quintana-Rodriguez E. et al.Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum.J. Ecol. 2015; 103: 250-260Crossref Scopus (0) Google Scholar]. In addition to their direct antimicrobial properties, such VOCs are known to trigger resistance responses in remote parts of the same plant or in neighboring plants [64Arimura G-I. et al.Herbivory-induced" @default.
- W1856292377 created "2016-06-24" @default.
- W1856292377 creator A5025634089 @default.
- W1856292377 creator A5044852686 @default.
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- W1856292377 date "2015-11-01" @default.
- W1856292377 modified "2023-10-16" @default.
- W1856292377 title "Optimizing Crops for Biocontrol of Pests and Disease" @default.
- W1856292377 cites W1499915383 @default.
- W1856292377 cites W1500788807 @default.
- W1856292377 cites W1525044524 @default.
- W1856292377 cites W1540177001 @default.
- W1856292377 cites W1543520056 @default.
- W1856292377 cites W1550833923 @default.
- W1856292377 cites W1556905261 @default.
- W1856292377 cites W1576318946 @default.
- W1856292377 cites W1595520263 @default.
- W1856292377 cites W1628574324 @default.
- W1856292377 cites W1654167775 @default.
- W1856292377 cites W1671008260 @default.
- W1856292377 cites W1846697969 @default.
- W1856292377 cites W1959427386 @default.
- W1856292377 cites W1963812953 @default.
- W1856292377 cites W1964918738 @default.
- W1856292377 cites W1966909275 @default.
- W1856292377 cites W1967034702 @default.
- W1856292377 cites W1967113476 @default.
- W1856292377 cites W1975391693 @default.
- W1856292377 cites W1980330188 @default.
- W1856292377 cites W1980346224 @default.
- W1856292377 cites W1982229803 @default.
- W1856292377 cites W1983239832 @default.
- W1856292377 cites W1984071969 @default.
- W1856292377 cites W1987723398 @default.
- W1856292377 cites W1987927621 @default.
- W1856292377 cites W1988824627 @default.
- W1856292377 cites W1989170176 @default.
- W1856292377 cites W1989442902 @default.
- W1856292377 cites W1991904567 @default.
- W1856292377 cites W1992398051 @default.
- W1856292377 cites W2000996508 @default.
- W1856292377 cites W2002242173 @default.
- W1856292377 cites W2004598930 @default.
- W1856292377 cites W2004737831 @default.
- W1856292377 cites W2005153249 @default.
- W1856292377 cites W2005906963 @default.
- W1856292377 cites W2010466554 @default.
- W1856292377 cites W2013968593 @default.
- W1856292377 cites W2016231934 @default.
- W1856292377 cites W2021902637 @default.
- W1856292377 cites W2023544981 @default.
- W1856292377 cites W2023921940 @default.
- W1856292377 cites W2024404140 @default.
- W1856292377 cites W2024633466 @default.
- W1856292377 cites W2026490476 @default.
- W1856292377 cites W2027251850 @default.
- W1856292377 cites W2028603584 @default.
- W1856292377 cites W2033487643 @default.
- W1856292377 cites W2037720131 @default.
- W1856292377 cites W2038463428 @default.
- W1856292377 cites W2039442876 @default.
- W1856292377 cites W2043739372 @default.
- W1856292377 cites W2045778189 @default.
- W1856292377 cites W2046363742 @default.
- W1856292377 cites W2046426068 @default.
- W1856292377 cites W2057737280 @default.
- W1856292377 cites W2058313118 @default.
- W1856292377 cites W2060637128 @default.
- W1856292377 cites W2063488615 @default.
- W1856292377 cites W2065874968 @default.
- W1856292377 cites W2071087800 @default.
- W1856292377 cites W2073596506 @default.
- W1856292377 cites W2075555797 @default.
- W1856292377 cites W2075922275 @default.
- W1856292377 cites W2080546742 @default.
- W1856292377 cites W2083408851 @default.
- W1856292377 cites W2085685120 @default.
- W1856292377 cites W2091585966 @default.
- W1856292377 cites W2096320882 @default.
- W1856292377 cites W2097646202 @default.
- W1856292377 cites W2098538114 @default.
- W1856292377 cites W2098688300 @default.
- W1856292377 cites W2100923668 @default.
- W1856292377 cites W2100953236 @default.
- W1856292377 cites W2103462627 @default.
- W1856292377 cites W2104980638 @default.
- W1856292377 cites W2105552974 @default.
- W1856292377 cites W2108099835 @default.
- W1856292377 cites W2108513093 @default.
- W1856292377 cites W2109856429 @default.
- W1856292377 cites W2112226358 @default.
- W1856292377 cites W2112742892 @default.
- W1856292377 cites W2113155026 @default.
- W1856292377 cites W2116811308 @default.
- W1856292377 cites W2120366835 @default.
- W1856292377 cites W2121309083 @default.
- W1856292377 cites W2122700505 @default.