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Plants emit a plethora of volatile organic compounds in response to biotic and abiotic stresses. These compounds act as infochemicals for ecological communication in the phytobiome. This study reviews the role of microbe-induced plant volatiles (MIPVs) in plant–microbe interactions. MIPVs are affected by the taxonomic position of the microbe, the identity of the plant and the type of interaction. Plants also emit exclusive blends of volatiles in response to nonhost and host interactions, as well as to beneficial microbes and necrotrophic/biotrophic pathogens. These MIPVs directly inhibit pathogen growth and indirectly promote resistance/susceptibility to subsequent plant pathogen attack. Viruses and phloem-limiting bacteria modify plant volatiles to attract insect vectors. Susceptible plants can respond to MIPVs from resistant plants and become resistant. Recent advances in our understanding of the molecular mechanisms of MIPV synthesis in plants and how plant pathogen effectors manipulate their biosynthesis are discussed. This knowledge will help broaden our understanding of plant–microbe interactions and should facilitate the development of new emerging techniques for sustainable plant disease management.

Herbivore-induced plant volatiles (HIPVs) are an important cue used in herbivore location by carnivorous arthropods such as parasitoids. The effects of plant volatiles on parasitoids have been well characterised at small spatial scales, but little research has been done on their effects at larger spatial scales. The spatial matrix of volatiles (‘volatile mosaic’) within which parasitoids locate their hosts is dynamic and heterogeneous. It is shaped by the spatial pattern of HIPV-emitting plants, the concentration, chemical composition and breakdown of the emitted HIPV blends, and by environmental factors such as wind, turbulence and vegetation that affect transport and mixing of odour plumes. The volatile mosaic may be exploited differentially by different parasitoid species, in relation to species traits such as sensory ability to perceive volatiles and the physical ability to move towards the source. Understanding how HIPVs influence parasitoids at larger spatial scales is crucial for our understanding of tritrophic interactions and sustainable pest management in agriculture. However, there is a large gap in our knowledge on how volatiles influence the process of host location by parasitoids at the landscape scale. Future studies should bridge the gap between the chemical and behavioural ecology of tritrophic interactions and landscape ecology.

The ability to predict future risks is essential for many organisms, including plants. Plants can gather information about potential future herbivory by detecting volatiles that are emitted by herbivore-attacked neighbors. Several individual volatiles have been identified as active danger cues. Recent work has also shown that plants may integrate multiple volatiles into their defense responses. Here, I discuss how the integration of multiple volatiles can increase the capacity of plants to predict future herbivore attack. I propose that integration of multiple volatile cues does not occur at the perception stage, but may through downstream early defense signaling and then be further consolidated by hormonal crosstalk. Exploring plant volatile cue integration can facilitate our understanding and utilization of chemical information transfer.

Herbivore‐induced plant volatiles (HIPVs) mediate critical ecological functions, but no studies have quantitatively synthesized data published on HIPVs to evaluate broad patterns. We tested three hypotheses that use eco‐evolutionary theory to predict volatile induction: feeding guild (chewing arthropods > sap feeders), diet breadth (specialist herbivores > generalists), and selection history (domesticated plants < wild species). To test these hypotheses, we extracted data from 236 experiments that report volatiles produced by herbivore‐damaged and undamaged plants. These data were subjected to meta‐analysis, including effects on total volatiles and major biochemical classes. Overall, we found that chewers induced more volatiles than sap feeders, for both total volatiles and most volatile classes (e.g. green leaf volatiles, monoterpenes). Although specialist herbivores induced more total volatiles than generalists, this was inconsistent across chemical classes. Contrary to our expectation, domesticated species induced stronger volatile responses than wild species, even when controlling for plant taxonomy. Surprisingly, this is the first quantitative synthesis of published studies on HIPVs. Our analysis provides support for perceptions in the published literature (chewers > sap feeders), while challenging other commonly held notions (wild > crop). Despite the large number of experiments, we identified several gaps in the existing literature that should guide future investigations.

Plants emit volatile blends specific to particular herbivore interactions, which predators and parasitoids learn to associate with prey, increasing herbivore mortality and thereby plant fitness in a phenomenon termed indirect defence. Herbivore‐induced plant volatile blends commonly include both rapid, transient green leaf volatiles (GLVs) and delayed, enduring sesquiterpenes. A few laboratory studies indicate that insects can use plant volatiles to time behaviour, but it is not known whether and how the temporal dynamics of plant volatile blends influence their function in indirect defence. We characterized the activity of the native herbivores Manduca sexta and Tupiocoris notatus and their predators, Geocoris spp., on their host plant Nicotiana attenuata in their natural habitat. Diurnal predator activity only partially overlapped with variable herbivore activity, and herbivore attack at the beginning or end of the photophase elicited plant volatile blends with distinct GLV and sesquiterpene profiles. In field trials, day‐active Geocoris spp. predators preferred morning‐ over evening‐typical GLV blends. Using plants genetically transformed so as to be unable to produce specific volatiles, we found that GLVs increased predation after dawn elicitations, whereas sesquiterpenes increased predation after dusk elicitations in field trials. We conclude that predators respond to temporal differences in plant volatile blends, and that the different dynamics of specific volatiles permit effective indirect defence despite variable herbivore activity in nature. A plain language summary is available for this article. Plain Language Summary

Summary Terpene synthases (TPSs) are key enzymes in terpenoids synthesis of plants and play crucial roles in regulating plant defence against pests and diseases. Here, we report the functional characterization of OsTPS19 and OsTPS20, which were upregulated by the attack of brown planthopper (BPH). BPH female adults performed concentration‐dependent behavioural responses to (S)‐limonene showing preference behaviour at low concentrations and avoidance behaviour at high concentrations. Overexpression lines of OsTPS19 and OsTPS20, which emitted higher amounts of the monoterpene (S)‐limonene, decreased the hatching rate of BPH eggs, reduced the lesion length of sheath blight caused by Rhizoctonia solani and bacterial blight caused by Xanthomonas oryzae. While knockout lines of OsTPS19 and OsTPS20, which emitted lower amounts of (S)‐limonene, were more susceptible to these pathogens. Overexpression of OsTPS19 and OsTPS20 in rice plants had adverse effects on the incidence of BPH, rice blast, and sheath blight in the field and had no significant impacts on rice yield traits. OsTPS19 and OsTPS20 were found to be involved in fine‐tuning the emission of (S)‐limonene in rice plants and play an important role in defence against both BPH and rice pathogens.

In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D. virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S. littoralis. We identified (E)-β-caryophyllene, which is induced by D. virgifera, and ethylene, which is suppressed by S. littoralis, as two signals used by D. virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.

Plants evolved strategies to attract pollinators that are essential for reproduction. However, plant defence against herbivores may trade off with pollinator attraction. Here, we investigated the role of inducible plant secondary metabolites in such a trade‐off. Our objective was to reveal the mechanisms underlying the effects of induced plant responses to pollination and herbivory. We assessed how responses of plants to pollination and insect herbivory affect the behaviour of flower visitors. Subsequently, we investigated how the production of volatile and non‐volatile compounds changes after pollination and herbivory. Both herbivores and pollinators induced important phenotypic changes in flowers. Brassica nigra plants respond to pollination and herbivory with changes in the profile of volatiles and non‐volatiles of their flowers. Our results show that butterflies use different cues when searching for an oviposition site or a nectar source. Pollination status influenced the behaviour of butterflies, but not that of syrphid flies. We discuss the results in the context of the trade‐off between defence and reproduction in plants and suggest that systemic responses to herbivores can interfere with local responses to pollination. Therefore, these responses must be addressed in an integrated way because, in nature, plants are simultaneously exposed to herbivores and pollinators.

Plants release herbivore‐induced volatiles (HIPVs), which can be used as cues by plants, herbivores and natural enemies. Theory predicts that HIPVs may initially have evolved because of their direct benefits for the emitter and were subsequently adopted as infochemicals. Here, we investigated the potential direct benefits of indole, a major HIPV constituent of many plant species and a key defence priming signal in maize. We used indole‐deficient maize mutants and synthetic indole at physiologically relevant doses to document the impact of the volatile on the generalist herbivore Spodoptera littoralis. Our experiments demonstrate that indole directly decreases food consumption, plant damage and survival of S. littoralis caterpillars. Surprisingly, exposure to volatile indole increased caterpillar growth. Furthermore, we show that S. littoralis caterpillars and adults consistently avoid indole‐producing plants in olfactometer experiments, feeding assays and oviposition trials. Synthesis. Together, these results provide a potential evolutionary trajectory by which the release of a HIPV as a direct defence precedes its use as a cue by herbivores and an alert signal by plants. Furthermore, our experiments show that the effects of a plant secondary metabolite on weight gain and food consumption can diverge in a counterintuitive manner, which implies that larval growth can be a poor proxy for herbivore fitness and plant resistance.

• Plant volatile emissions can recruit predators of herbivores for indirect defense and attract pollinators to aid in pollination. Although volatiles involved in defense and pollinator attraction are primarily emitted from leaves and flowers, respectively, they will co-evolve if their underlying genetic basis is intrinsically linked, due either to pleiotropy or to genetic linkage. However, direct evidence of co-evolving defense and floral traits is scarce. • We characterized intraspecific variation of herbivory-induced plant volatiles (HIPVs), the key components of indirect defense against herbivores, and floral volatiles in wild tobacco Nicotiana attenuata. • We found that variation of (E)-β-ocimene and (E)-α-bergamotene contributed to the correlated changes in HIPVs and floral volatiles among N. attenuata natural accessions. Intraspecific variations of (E)-β-ocimene and (E)-α-bergamotene emissions resulted from allelic variation of two genetically co-localized terpene synthase genes, NaTPS25 and NaTPS38, respectively. Analyzing haplotypes of NaTPS25 and NaTPS38 revealed that allelic variations of NaTPS25 and NaTPS38 resulted in correlated changes of (E)-β-ocimene and (E)-α-bergamotene emission in HIPVs and floral volatiles in N. attenuata. • Together, these results provide evidence that pleiotropy and genetic linkage result in correlated changes in defenses and floral signals in natural populations, and the evolution of plant volatiles is probably under diffuse selection.