Changed host plant volatile emissions induced by chemical interaction between unattacked plants reduce aphid plant acceptance with intermorph variation (original) (raw)
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Journal of Pest Science, 2023
Recent studies have demonstrated that cultivar mixtures can reduce aphid plant acceptance and population development. It is still unknown as to which underlying mechanisms may contribute to this phenomenon. We investigated the effects of volatile interactions between undamaged barley cultivars on aphid feeding behavior and performance in the laboratory. Spring barley (Hordeum vulgare L.) cultivar Salome was exposed to volatiles from Fairytale (SeF), Anakin (SeA), or clean air (Se0). We used an electrical penetration graph to test the effect of exposure to neighbor volatiles on the feeding behavior and performance of bird cherry-oat aphids (Rhopalosiphum padi L.). We also assessed aphid relative growth rate, intrinsic rate of increase, and development time on exposed and unexposed Salome plants. Aphids spent significantly longer time on epidermis and mesophyll plant tissues on SeF than Se0, and no difference was observed between SeA and Se0. Significant decreases in the duration of phloem ingestion and phloem sustained ingestion were recorded in SeF showing that volatileinduced effects cause difficulty for aphids to feed. However, no differences in these variables were detected between SeA and Se0. We also observed reduced aphid relative growth rate and intrinsic rate of increase on SeF compared to Se0 and SeA. Our study demonstrated that, in a specific combination, exposure of one barley cultivar to volatiles from another one can change aphid feeding behavior and performance, probably due to changes in host plant properties/quality. Our results provide an insightful explanation of mechanisms responsible for the reduced aphid population development previously observed in the field. Keywords Variety mixture • Plant-plant interactions • Plant-insect interactions • Plant protection • Induced defense • EPG Key messages • Volatile interactions between undamaged barley cultivars disrupt aphid feeding behavior and reduce aphid relative growth rate and intrinsic rate. • Volatile-induced responses in plants, which affect aphid feeding and performance, depend on the genotype of the neighboring cultivar. • Volatile interactions between specific cultivars could be the underlying mechanism, which reduces aphid population development in cultivar mixtures in the field.
Herbivore-induced plant volatiles provide foraging cues for herbivores and for herbivores' natural enemies. Aphids induce plant volatile emissions and also utilize plant-derived olfactory volatile cues, but the chemical ecology of aphids and other phloem-feeding insects is less extensively documented than that of chewing insects. Here, we characterize the volatile cues emitted by turnip plants (Brassica rapa) under attack by an aphid (Myzus persicae) or by the chewing lepidopteran larva Heliothis virescens. We also tested the behavioral responses of M. persicae individuals to the odors of undamaged and herbivore-damaged plants presented singly or in combination, as well as to the odor of crushed conspecifics (simulating predation). Gas chromatographic analysis of the volatile blend of infested turnips revealed distinct profiles for both aphid-and caterpillar-induced plants, with induced compounds including green-leaf alcohols, esters, and isothiocyanates. In behavioral trials, aphids exhibited increased activity in the presence of plant odors and positive attraction to undamaged turnip plants. However, aphids exhibited a strong preference for the odors of healthy versus plants subjected to herbivore damage, and neither aphid-or caterpillar-damaged plants were attractive compared to clean-air controls. Reduced aphid attraction to herbivore-infested plants may be mediated by changes in the volatile blend constituent composition, including large amounts of isothiocyanates and green-leaf volatiles or, in the case of aphid-infested plants, of the aphid alarm pheromone, (E)-b-farnesene.
Host-locating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles
Journal of Plant Interactions, 2007
The blend of volatile compounds emitted by tomato plants (Solanum lycopersicum) infested with the potato aphid (Macrosiphum euphorbiae) has been studied comparatively with undamaged plants and aphids themselves. Aphid-infested plants were significantly more attractive towards Aphidius ervi than undamaged plants and aphids themselves. Oriented response towards host-damaged plant, from which aphids were removed just before running the bioassay, did not differ from that recorded for infested plants. Collection of the volatiles and analysis by gas chromatography revealed only quantitative differences between uninfested and aphid-infested plants. Nine compounds, a-pinene, (Z)-3-hexen-1-ol, a-phellandrene, limonene, (E)-b-ocimene, p-cymene, methyl salicylate, (E)-b-caryophyllene and an unknown compound, were emitted at higher levels from aphid-infested plants than from undamaged control plants, whilst no differences were noted for hexanal, 6-methyl-5-hepten-2-one, and humulene (0a-caryophyllene). Synthetic standards of these compounds were tested in wind tunnel bioassays and all elicited a significant increase in oriented flight and landings on the target by the aphid parasitoid Aphidius ervi. (E)-b-caryophyllene resulted the most attractive towards female wasps. These results corroborate the hypothesis that the volatiles produced by the plant in response to aphid attack derive from both jasmonic and salicylic acid pathways, and are exploited by A. ervi as olfactory cues to locate its hosts.
Learning of plant volatiles by aphid parasitoids: timing to learn
Journal of Plant Interactions, 2011
One of the intriguing questions in insectÁplant interaction is how parasitic wasps exploit host herbivore-induced plant volatiles (HIPVs) to find a micro-host habitat (i.e. host-infested plants) that copes with the variation of HIPVs. Associative learning of host-related HIPVs is one of the solutions. Here, we reviewed parasitic wasps of aphids learning a specific blend of HIPVs. Their timing of learning was either (1) learning after emergence, (2) learning at the emergence, or (3) learning at larval and/or pre-pupal stages.
PLoS ONE, 2013
Changes in plant volatile emission can be induced by exposure to volatiles from neighbouring insect-attacked plants. However, plants are also exposed to volatiles from unattacked neighbours, and the consequences of this have not been explored. We investigated whether volatile exchange between undamaged plants affects volatile emission and plant-insect interaction. Consistently greater quantities of two terpenoids were found in the headspace of potato previously exposed to volatiles from undamaged onion plants identified by mass spectrometry. Using live plants and synthetic blends mimicking exposed and unexposed potato, we tested the olfactory response of winged aphids, Myzus persicae. The altered potato volatile profile deterred aphids in laboratory experiments. Further, we show that growing potato together with onion in the field reduces the abundance of winged, host-seeking aphids. Our study broadens the ecological significance of the phenomenon; volatiles carry not only information on whether or not neighbouring plants are under attack, but also information on the emitter plants themselves. In this way responding plants could obtain information on whether the neighbouring plant is a competitive threat and can accordingly adjust their growth towards it. We interpret this as a response in the process of adaptation towards neighbouring plants. Furthermore, these physiological changes in the responding plants have significant ecological impact, as behaviour of aphids was affected. Since herbivore host plants are potentially under constant exposure to these volatiles, our study has major implications for the understanding of how mechanisms within plant communities affect insects. This knowledge could be used to improve plant protection and increase scientific understanding of communication between plants and its impact on other organisms.
The Science of Nature, 2021
The use of nectar-producing companion plants in crops is a well-known strategy of conserving natural enemies in biological control. However, the role of floral volatiles in attracting parasitoids and effects on host location via herbivore-induced plant volatiles is poorly known. Here, we examined the role of floral volatiles from marigold (Tagetes erecta), alone or in combination with volatiles from sweet pepper plant (Capsicum annuum), in recruiting Aphidius platensis, an important parasitoid of the green peach aphid Myzus persicae. We also investigated whether marigold floral volatiles are more attractive to the parasitoid than those emitted by sweet pepper plants infested by M. persicae. Olfactometry assays indicated that floral volatiles attracted A. platensis to the marigold plant and are more attractive than sweet pepper plant volatiles. However, volatiles emitted by aphid-infested sweet pepper were as attractive to the parasitoid as those of uninfested or aphid-infested blooming marigold. The composition of volatile blends released by uninfested and aphid-infested plants differed between both blooming marigold and sweet pepper, but the parasitoid did not discriminate aphid-infested from uninfested blooming marigold. Volatile released from blooming marigold and sweet pepper shared several compounds, but that of blooming marigold contained larger amounts of fatty-acid derivatives and a different composition of terpenes. We discuss the potential implications of the aphid parasitoid attraction in a diversified crop management strategy.
Alterations in the odor profile of plants in cultivar mixtures affect aphid host-location behavior
Frontiers in Plant Science, 2023
The effect of cultivar mixtures on aphid control is attributed to the masking or alteration of host-preferred cultivar odor cues. However, the underlying physiological mechanism remains unclear. This study assessed alterations in the volatile emissions of wheat cultivars grown together (Florence-Aurora and Forment; Florence-Aurora and Montcada) and the consequences for the olfactory preference of aphids. Volatile organic compounds were collected from wheat plants grown in a laboratory under mixed or monoculture conditions and subsequently analyzed. The odor profiles of Florence-Aurora and Montcada were indistinguishable from each other. However, the odors of Florence-Aurora and Forment grown in monocultures differed significantly from those emitted by their mixture. The Florence-Aurora and Forment mixture induced plant physiological responses that affected the emission of single volatile compounds and, consequently, altered volatile organic compound ratios. English grain aphids (Sitobion avenae) were less attracted to the odors of Florence-Aurora and Forment when grown as a mixture than the combination of the odors from Florence-Aurora and Forment monocultures. Moreover, aphids preferred clean air over the odor from the Florence-Aurora and Forment mixture but preferred the odor from the Florence-Aurora and Montcada mixture over clean air. This study highlights the beneficial effects of intraspecific plant diversity on aphid control by altering plant odors in response to plant-plant interactions. The emission of less attractive odor cues consequently affects plant-aphid interactions; hence, less attractive odors are likely to impair aphid host-locating behavior. This effect was exclusive to certain cultivar mixtures, which supports the "right neighbor" concept.
Interactions between tomato volatile organic compounds and aphid behaviour
Journal of Plant Interactions, 2012
In the tritrophic system consisting of tomato, Solanum lycopersicum (L.), the aphid Macrosiphum euphorbiae (Thomas) and its natural enemy, the parasitoid Aphidius ervi (Haliday), it has been shown that the release of volatile organic compounds following aphid attack is responsible for attracting aphid parasitoids in wind tunnel experiments. The main compounds involved in these multitrophic interactions have been characterized and quantified. In this work, the possible activity of such compounds on plant direct defences against the aphid M. euphorbiae was assessed in laboratory tests. The selected compounds were applied to uninfested tomato plants, either by evaporation or contact, and performance of aphids, in terms of plant acceptance, fixing behaviour and aphid development, calculated in standard conditions. The results showed that two compounds, namely methyl salicylate and cis-hex-3-en-1-ol, alter aphid performance. These two compounds have been reported to be those eliciting the best response by A. ervi in terms of flight behavior (wind tunnel bioassay) and antennal stimulation (EAG bioassay).