Evolution of signal emission by non-infested plants growing near infested plants to avoid future risk

Several plant species indirectly defend themselves against herbivory by attracting natural enemies of herbivores by releasing signal chemicals when infested. Previous empirical research suggested that the chemical signals also reflexively induce signal emission by neighboring undamaged plants. We hypothesize that such a reflexively induced signal is a defensive strategy used by undamaged plants to avoid possible future risk. Using a mathematical model, we show that this defense against future risk can evolve if the following conditions are met: (1) the cost of the signal is small relative to the cost of damage by infestation, (2) the attractiveness of the signal to natural enemies is positively correlated with the local density of the signal chemical, (3) plants with infested neighbors are at greater risk than those without infested neighbors, and (4) the lifespan of plants is long compared with that of herbivores. We also discuss the relationship between our model and recent models of the evolution of cooperation.     

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), Female Moths Respond to Herbivore-Induced Corn Volatiles

In response to herbivore attack, plants release herbivore-induced plant volatiles (HIPVs) that represent important chemical cues for herbivore natural enemies. Additionally, HIPVs have been shown to mediate other ecological interactions with herbivores. Differently from natural enemies that are generally attracted to HIPVs, herbivores can be either attracted or repelled depending on several biological and ecological parameters. Our study aimed to assess the olfactory response of fall armyworm-mated female moths toward odors released by mechanically and herbivore-induced corn at different time intervals. Results showed that female moths strongly respond to corn volatiles, although fresh damaged corn odors (0?C1?h) are not recognized by moths. Moreover, females preferred volatiles released by undamaged plant over herbivore-induced plants at 5?C6?h. This preference for undamaged plants may reflect an adaptive strategy of moths to avoid competitors and natural enemies for their offspring. We discussed our results based on knowledge about corn volatile release pattern and raise possible explanations for fall armyworm moth behavior.     

Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles

Plants damaged by herbivores emit blends of volatile organic compounds (VOCs) that attract the herbivore’s natural enemies. Most work has focussed on systems involving one plant, one herbivore and one natural enemy, though, in nature, plants support multiple herbivores and multiple natural enemies of these herbivores. Our study aimed to understand how different aphid natural enemies respond to aphid-induced VOCs, and whether attraction of the natural enemies that responded to aphid-induced VOCs was altered by simultaneous damage by a chewing herbivore. We used a model system based on Brassica juncea (Brassicaceae), Myzus persicae (Hemiptera: Aphididae) and Plutella xylostella (Lepidoptera: Plutellidae). Ceraeochrysa cubana (Neuroptera: Chrysopidae) did not show preferences for any plant odour, while Cycloneda sanguinea (Coleoptera: Coccinellidae) responded to undamaged plants over air but not to aphid-damaged plants over undamaged plants. Therefore, no further tests were carried out with these two species. Chrysoperla externa (Neuroptera: Chrysopidae) preferred aphid-damaged plants, but not caterpillar-damaged plants, over undamaged plants, and preferred plants damaged by both herbivores over both undamaged plants and aphid-damaged plants. When tested for responses against undamaged plants, Aphidius colemani (Hymenoptera: Braconidae) preferred aphid-damaged plants but not plants damaged by caterpillars. Plants damaged by both herbivores attracted more parasitoids than undamaged plants, but not more than aphid-damaged plants. Thus, multiply damaged plants were equally attractive to A. colemani and more attractive to C. externa than aphid-damaged plants, while C. cubana and C. sanguinea did not respond to aphid-induced VOCs, highlighting how different natural enemies can have different responses to herbivore-damaged plants.     

Evolution of talking plants in a tritrophic context: conditions for uninfested plants to attract predators prior to herbivore attack

Herbivory induces plants to emit volatile chemicals that attract enemies of the herbivores (bodyguards of plants). In this way, the plant acquires protection and the bodyguards gain food. These plant signals cause neighboring plants, not under attack, to release signals as well. We hypothesize that such "secondary" signals help to reduce damage from future herbivore attacks by the protection received from the bodyguards. By modeling we explore the conditions for such secondary signals to evolve. Three kinds of strategies are considered: plants of the first strategy always emit a signal, those of the second strategy emit a signal only when infested, and those of the third strategy emit a signal not only when infested, but also when a certain number of neighbors are infested (i.e. secondary signaling). When signaling is much less (much more) costly than damage from herbivory, the first (second) strategy will be favored by selection, whereas for intermediate costs the third strategy, i.e. secondary signaling, will evolve. However, secondary signaling will not evolve when the primary signals lure the bodyguards too effectively. This is because the undamaged plant gains associational defense when the infested individual is defending very well; therefore, the need for secondary signaling decreases.     

No evidence of modulation of indirect plant resistance of Brassica rapa plants by volatiles from soil-borne fungi

1. Upon herbivory, plants emit specific herbivore-induced plant volatiles (HIPVs) that can attract natural enemies of the herbivore thus serving as indirect plant resistance. Not only insect herbivores, but microorganisms may also affect HIPV emission before or after plant colonisation, which in turn can affect behaviour of natural enemies of the herbivore. Yet, it remains elusive whether volatiles from microorganisms influence HIPV emission and indirect plant resistance.
2. In this study, we investigated whether exposure of Brassica rapa roots to volatiles from soil-borne fungi influence HIPV emission and the recruitment of natural enemies of Pieris brassicae larvae.
3. Using a two-compartment pot system, we performed greenhouse and common-garden experiments, and we profiled plant HIPV emission.
4. We found that exposure of plant roots to fungal volatiles did not affect the number of P. brassicae larvae recollected from the plants, suggesting a neutral effect of the fungal volatiles on natural predation. Likewise, in a greenhouse, similar numbers of larvae were parasitised by Cotesia glomerata wasps on control plants as on fungal volatile-exposed plants. Additionally, chemical analysis of HIPV profiles revealed no qualitative and quantitative differences between control plants and fungal volatile-exposed plants that were both infested with P. brassicae larvae.
5. Together, our data indicate that root exposure to fungal volatiles did not affect indirect plant resistance to an insect herbivore. These findings provide new insight into the influence of indirect plant resistance by fungal volatiles that are discussed together with the effects of fungal volatiles on direct plant resistance.

     

Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests

In response to feeding by arthropods, plants actively and systemically emit various volatile substances. It has been proposed that these herbivore-induced volatiles (HIPVs) can be exploited in agricultural pest control because they might repel herbivores and because they serve as attractants for the enemies of the herbivores. Indeed, recent studies with transgenic plants confirm that odour emissions can be manipulated in order to enhance the plants' attractiveness to beneficial arthropods. An additional advantage of manipulating HIPV emissions could be their effects on neighbouring plants, as a rapidly increasing number of studies show that exposure to HIPVs primes plants for augmented defence expression. Targeting the right volatiles for enhanced emission should lead to ecologically and economically sound ways of combating important pests.     

Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks

In response to feeding by phytophagous arthropods, plants emit volatile chemicals. This is shown to be an active physiological response of the plant and the released chemicals are therefore called herbivore-induced plant volatiles (HIPV). One of the supposed functions of HIPV for the plant is to attract carnivorous natural enemies of herbivores. Depending on which plant and herbivore species interact, blends of HIPV show qualitative and quantitative variation. Hence, one may ask whether this allows the natural enemies to discriminate between volatiles from plants infested by herbivore species that are either suitable or unsuitable as a food source for the natural enemy. Another question is whether natural enemies can also recognise HIPV when two or more herbivore species that differ in suitability as a food source simultaneously attack the same plant species. By reviewing the literature we show that arthropod predators and parasitoids can tell different HIPV blends apart in several cases of single plant–single herbivore systems and even in single plant–multiple herbivore systems. Yet, there are also cases where predators and parasitoids do not discriminate or discriminate only after having learned the association between HIPV and herbivores that are either suitable or non-suitable as a source of food. In this case, suitable herbivores may profit from colonising plants that are already infested by another non-suitable herbivore. The resulting temporal or partial refuge may have important population dynamical consequences, as such refuges have been shown to stabilise otherwise unstable predator–prey models of the Lotka-Volterra or Nicholson-Bailey type.     

虫害诱导的植物挥发物代谢调控机制研究进展

长期受自然界的非生物/生物侵害,植物逐步形成了复杂的防御机制,为防御植食性昆虫的为害,植物释放虫害诱导产生的挥发性化合物(herbivore-induced plant volatiles,HIPVs)。HIPVs是植物-植食性昆虫-天敌三级营养关系之间协同进化的结果。HIPVs的化学组分因植物、植食性昆虫种类的不同而有差异。生态系统中,HIPVs可在植物与节肢动物、植物与微生物、虫害植物与邻近的健康植物、或同一植株的受害和未受害部位间起作用,介导防御性反应。HIPVs作为寄主定位信号,在吸引捕食性、寄生性天敌过程中起着重要作用。HIPVs还可以作为植物间信息交流的工具,启动植株的防御反应而增强抗虫性。不论从生态学还是经济学角度来看,HIPVs对于农林生态系中害虫综合治理策略的完善具有重要意义。前期的研究在虫害诱导植物防御的化学生态学方面奠定了良好基础,目前更多的研究转向阐述虫害诱导植物抗性的分子机制。为了深入了解HIPVs的代谢调控机制,主要从以下几个方面进行了综述。因为植食性昆虫取食造成的植物损伤是与昆虫口腔分泌物共同作用的结果,所以首先阐述口腔分泌物在防御反应中的作用。挥发物诱导素volicitin和β-葡萄糖苷酶作为口腔分泌物的组分,是产生HIPVs的激发子,通过调节伤信号诱发HIPVs的释放。接着阐述了信号转导途径对HIPVs释放的调节作用,并讨论了不同信号途径之间的交互作用。就HIPVs的代谢过程而言,其过程受信号转导途径(包括茉莉酸、水杨酸、乙烯、过氧化氢信号途径)的调控,其中茉莉酸信号途径是诱发HIPVs释放的重要途径。基于前人的研究,综述了HIPVs的主要代谢过程及其过程中关键酶类的调控作用。文中的HIPVs主要包括萜烯类化合物、绿叶挥发物和莽草酸途径产生的芳香族化合物,如水杨酸甲酯和吲哚等。作为化学信号分子,这些化合物中的一部分还能激活邻近植物防御基因的表达。萜烯合酶是各种萜烯类化合物合成的关键酶类,脂氧合酶、过氧化氢裂解酶也是绿叶挥发物代谢途径中的研究热点,而苯丙氨酸裂解酶和水杨酸羧基甲基转移酶分别是合成水杨酸及其衍生物水杨酸甲酯的关键酶类。这些酶类的基因在转录水平上调控着HIPVs代谢途径。最后展望了HIPVs的研究前景。     

Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles

Feeding damage to plants by insect herbivores induces the production of plant volatiles, which are attractive to the herbivores natural enemies. Little is understood about the plant biochemical pathways involved in aphid-induced plant volatile production. The aphid parasitoid Diaeretiella rapae can detect and respond to aphid-induced volatiles produced by Arabidopsis thaliana. When given experience of those volatiles, it can learn those cues and can therefore be used as a novel biosensor to detect them. The pathways involved in aphid-induced volatile production were investigated by comparing the responses of D. rapae to volatiles from a number of different transgenic mutants of A. thaliana, mutated in their octadecanoid, ethylene or salicylic acid wound-response pathways and also from wild-type plants. Plants were either undamaged or infested by the peach-potato aphid, Myzus persicae. It is demonstrated that the octadecanoid pathway and specifically the COI1 gene are required for aphid-induced volatile production. The presence of salicylic acid is also involved in volatile production. Using this model system, in combination with A. thaliana plants with single point gene mutations, has potential for the precise dissection of biochemical pathways involved in the production of aphid-induced volatiles.     

Plant volatiles as method of communication

Plants emit volatile compounds that can act as a communication method to insects, neighboring plants and pathogens. Plants respond to leaf and root damage by herbivores and pathogens by emitting these compounds. The volatile compounds can deter the herbivores or pathogens directly or indirectly by attracting their natural enemies to kill them. The simultaneous damage of plants by herbivores and pathogens can influence plant defense. The induced plant volatiles can also make neighboring plants ready for defense or induce defense in parts distant from the damaged area of the same plant. Belowground root herbivory can alter the defense response to aboveground leaf herbivory. In addition, most plants normally emit volatile compounds from their flowers that directly attract foraging mutualistic insects for nectar, which in turn perform the very important function of pollination for subsequent reproduction. The volatile compounds emitted from the floral and vegetative parts of plants belong to three main classes of compounds: terpenoids, phenylpropanoids/benzenoids, and C6-aldehydes (green-leaf volatiles). The volatile phytohormones methyl salicylate and methyl jasmonate serve as important signaling molecules for communication purposes, and interact with each other to optimize the plant defense response. Here we discuss and integrate the current knowledge on all types of communication between plants and insects, neighboring plants and pathogens that are mediated through plant volatiles.     

Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies

Herbivore-damaged plants emit volatile organic compounds that attract natural enemies of the herbivores. This form of indirect plant defence occurs aboveground as well as belowground, but it remains unclear how simultaneous feeding by different herbivores attacking leaves and roots may affect the production of the respective defence signals. We employed a setup that combines trapping of volatile organic signals and simultaneous measurements of the attractiveness of these signals to above and belowground natural enemies. Young maize plants were infested with either the foliar herbivore Spodoptera littoralis , the root herbivore Diabrotica virgifera virgifera , or with both these important pest insects. The parasitic wasp Cotesia marginiventris and the entomopathogenic nematode Heterorhabditis megidis were strongly attracted if their respective host was feeding on a plant, but this attraction was significantly reduced if both herbivores were on a plant. The emission of the principal root attractant was indeed reduced due to double infestation, but this was not evident for the leaf volatiles. The parasitoid showed an ability to learn the differences in odour emissions and increased its response to the odour of a doubly infested plant after experiencing this odour during an encounter with hosts. This first study to measure effects of belowground herbivory on aboveground tritrophic signalling and vice-versa reemphasizes the important role of plants in bridging interactions between spatially distinct components of the ecosystem.     

The formation and function of plant volatiles: perfumes for pollinator attraction and defense

Plants synthesize and emit a large variety of volatile organic compounds with terpenoids and fatty-acid derivatives the dominant classes. Whereas some volatiles are probably common to almost all plants, others are specific to only one or a few related taxa. The rapid progress in elucidating the biosynthetic pathways, enzymes, and genes involved in the formation of plant volatiles allows their physiology and function to be rigorously investigated at the molecular and biochemical levels. Floral volatiles serve as attractants for species-specific pollinators, whereas the volatiles emitted from vegetative parts, especially those released after herbivory, appear to protect plants by deterring herbivores and by attracting the enemies of herbivores.     

Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores

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)-β-farnesene.     

Genetic variation in plant volatile emission does not result in differential attraction of natural enemies in the field

Volatile organic chemical (VOC) emission by plants may serve as an adaptive plant defense by attracting the natural enemies of herbivores. For plant VOC emission to evolve as an adaptive defense, plants must show genetic variability for the trait. To date, such variability has been investigated primarily in agricultural systems, yet relatively little is known about genetic variation in VOCs emitted by natural populations of native plants. Here, we investigate intraspecific variation in constitutive and herbivore-induced plant VOC emission using the native common milkweed plant (Asclepias syriaca) and its monarch caterpillar herbivore (Danaus plexippus) in complementary field and common garden greenhouse experiments. In addition, we used a common garden field experiment to gauge natural enemy attraction to milkweed VOCs induced by monarch damage. We found evidence of genetic variation in the total constitutive and induced concentrations of VOCs and the composition of VOC blends emitted by milkweed plants. However, all milkweed genotypes responded similarly to induction by monarchs in terms of their relative change in VOC concentration and blend. Natural enemies attacked decoy caterpillars more frequently on damaged than on undamaged milkweed, and natural enemy visitation was associated with higher total VOC concentrations and with VOC blend. Thus, we present evidence that induced VOCs emitted by milkweed may function as a defense against herbivores. However, plant genotypes were equally attractive to natural enemies. Although milkweed genotypes diverge phenotypically in their VOC concentrations and blends, they converge into similar phenotypes with regard to magnitude of induction and enemy attraction.     

Behavioural responses of the aphid parasitoid Diaeretiella rapae to volatiles from Arabidopsis thaliana induced by Myzus persicae

In response to herbivory by insects, several plant species have been shown to produce volatiles that attract the natural enemies of those herbivores. Using a Y‐tube olfactometer, we investigated responses of the aphid parasitoid Diaeretiella rapae MacIntosh (Hymenoptera: Aphidiidae) to volatiles from Arabidopsis thaliana Columbia (Brassicaceae) plants that were either undamaged, infested by the peach‐potato aphid, Myzus persicae Sulzer (Homoptera: Aphididae), or mechanically damaged, as well as to volatiles from just the aphid or its honeydew. In dual‐choice experiments, female D. rapae given oviposition experience on A. thaliana infested with M. persicae were significantly attracted to volatiles from A. thaliana infested with M. persicae over volatiles from undamaged A. thaliana and similarly were significantly attracted to plants that had been previously infested by M. persicae, but from which the aphids were removed, over undamaged plants. Diaeretiella rapae did not respond to volatiles from M. persicae alone, their honeydew, or plants mechanically damaged with either a pin or scissors. We conclude that an interaction between the plant and the aphid induces A. thaliana to produce volatiles, which D. rapae can learn and respond to. Poor responses of D. rapae to volatiles from an A. thaliana plant that had two leaves infested with M. persicae, with the two infested leaves being removed before testing, suggested the possibility that, at this stage of infestation, the majority of volatile production induced by M. persicae may be localized to the infested tissues of the plant. We conclude that this tritrophic interaction is a suitable model system for future investigations of the biochemical pathways involved in the production of aphid‐induced volatiles attractive to natural enemies.     

Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata , a parasitoid of the leaf herbivore Pieris brassicae , mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.     

虫害诱导植物挥发物(HIPVs)对植食性昆虫的行为调控

虫害诱导植物挥发物(herbivore induced plant volatiles,HIPVs)具有植物种类、品种、生育期和部位的特异性,也具有植食性昆虫种类、虫龄、为害程度、为害方式和其他一些环境因子的特异性。由于其释放量明显大于健康植株,因此更易被天敌、害虫以及邻近的植物等所利用,从而调节植物、植食性昆虫与天敌三者之间的相互作用关系,增强植物在自然界的生存竞争能力。本文对HIPVs在植食性昆虫寄主定位行为中的作用、HIPVs对植食性昆虫的种群调控功能及其应用现状2个方面加以综述,并在展望中对目前研究中存在的一些问题进行了探讨。     

Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions

Recent research bridging mechanistic and ecological approaches demonstrates that plant attributes can affect herbivores, natural enemies of herbivores, and their interaction. Such effects may be genetically variable among plants and/or induced in individual plants by herbivore attack, and are mediated by primary plant attributes (i.e. nutritional quality and physical structure) and defense-related products (i.e. secondary chemicals and plant volatiles), and may be modified by human activity (e.g. by the introduction of Bacillus thuringiensis). The study of tri-trophic interactions is important in order to understand natural species interactions and to manipulate these interactions in pest control.     

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

Maize plants respond to feeding by arthropod herbivores by producing a number of secondary plant compounds, including volatile organic compounds (VOCs). These herbivore-induced VOCs are not only known to attract natural enemies of the herbivores, but they may also prime inducible defences in neighbouring plants, resulting in stronger and faster defence responses in these VOC-exposed plants. Among the compounds that cause this priming effect, green leaf volatiles (GLVs) have received particular attention, as they are ubiquitous and rapidly emitted upon damage. In this study, we investigated their effects under realistic conditions by applying specially devised dispensers to release four synthetic GLVs at physiologically relevant concentrations in a series of experiments in maize fields. We compared the VOC emission of GLV-exposed maize plants to non-exposed plants and monitored the attraction of herbivores and predators, as well as parasitism of the caterpillar Spodoptera frugiperda, the most common herbivore in the experimental maize fields. We found that maize plants that were exposed to GLVs emitted increased quantities of sesquiterpenes compared to non-exposed plants. In several replicates, herbivorous insects, such as adult Diabrotica beetles and S. frugiperda larvae, were observed more frequently in GLV-treated plots and caused more damage to GLV-exposed plants than to non-exposed plants. Parasitism of S. frugiperda was only weakly affected by GLVs and overall parasitism rates of S. frugiperda were similar in GLV-exposed and non-exposed plots. The effects on insect presence depended on the distance from the GLV-dispensers at which the plants were located. The results are discussed in the context of strategies to improve biological control by enhancing plant-mediated attraction of natural enemies.